The effects of familiarization with loading,weight and size of loading on neuromuscular responses during sudden upper limb loading in chronic low back pain patients

2.1 Study population

We enrolled 7 men and 13 women with CLBP as well as 20 asymptomatic subjects (10 men and 10 women) aged 18–45 years, who were recruited through leaflet advertising [18]. Because more women agreed to participate in the study sooner, both genders were not equally distributed. The two groups were matched by age, height, and weight. Any pain, tenderness, or discomfort between the edge of the twelfth ribs and the gluteal folds for three or more months [19, 20, 21], VAS ⩽ 3 [21], and the absence of any lumbar radicular signs were the inclusion criteria for the LBP patients [22]. In addition, the absence of any respiratory, neurological, or orthopedic conditions was also an inclusion criterion for the asymptomatic subjects [23]. Participants were excluded if they were unwilling to continue the test and if the pain exacerbated during the test (Appendix).

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This quasi-experimental study was performed as described in Fig. 1. The correct posture was defined as standing over the force plate with the knees completely extended and elbows flexed at 90 ∘ with a basket in the hands, the ears covered, and the eyes either closed or open. Three boxes were used in this research as loads (1 – a small box weighing 1% of the subject’s body mass, 2 – a small box weighing 2% of the subject’s body mass, 3 – a large box weighing 2% of the subject’s body mass). An electromagnetic system was used to fix these boxes approximately at eye level, directly above the basket. In each condition, any one of the above boxes was released at a random time into the basket without warning [23]. All trials were done with the eyes open. The impact time was indicated with a marker switch in the basket. Figure 1 illustrates the study procedure. The Tehran University of Medical Sciences Ethics Board approved this study (Ethical code: 130/3428; date: 18/3/2013), and it was performed according to the principles of the Declaration of Helsinki.

2.3 Electromyography and force plate recordings

Surface Electromyography (EMG) was conducted using the ME 6000 (Mega Electronics Ltd. Kuopio, Finland). EMG of the muscles on the right and the left sides was recorded after the subjects’ skin was prepared by shaving, rubbing, and cleaning with alcohol pads. The middle points of each pair of the surface EMG electrodes (Ag-AgCl discs) were then placed as follows: transversusabdominus/internal oblique (TrA/IO) approximately 2 cm medial and inferior to the anterior superior iliac spine [24], the external oblique (EOA) 10 cm lateral to the umbilicus with a 45 ∘ vertical orientation [25], and the ES muscle at the L3–L4 level approximately 4 cm lateral from the midline. The longitudinally oriented electrodes along the fibers of the muscle were positioned with a center-to-center electrode distance of 2.5 cm [26]. Band-pass filtering and sampling of the EMG data were performed between 20 Hz and 500 [27, 28] using Qualisys Track Manager software version 2.7 (QTM, Gothenburg, Sweden). In addition, data were exported to MATLAB software version 7 (MathWorks, USA) for analyses. A time window of 200 ms before and 250 ms after perturbation was considered for the analysis [28]. Normalization of the root-mean-square (RMS) of the EMG signal was performed according to the method used by Kanekar et al. [29] and Silfies et al. [30]. Consequently, using the MATLAB software, the integral of the EMG signal (IEMG) representing muscle activity and the muscle onset latencies were calculated. Muscle onset was defined as the point when the RMS signal crossed the threshold of the mean plus three standard deviations of the pre-perturbation baseline signals. Crossing the threshold for at least 20 ms was considered as muscle onset to avoid misinterpreting an EMG spike activity as muscle onset during signal processing [28].

A force plate device to assess control of the posture (Kistler Company, Switzerland) was used to measure the Fz (vertical component of ground reaction force), peak latency (time to peak of the muscle electrical activity), the total center of pressure (COP) excursion, and COP excursion along the Y axis (YCOP). The data from the EMG systems, marker switch, and the force plate were collected synchronously [31].

2.4 Statistical analyses

Data analyses were performed using SPSS software version 18 (SPSS Inc. Chicago, USA). The normality of the data was examined using the Kolmogorov-Smirnov test. Paired t -tests were used to calculate the within-group differences following studied conditions. Independent t -tests were used to calculate the between-group differences in the studied conditions. For the force and COP data, the mean value of the three measurements and for the EMG data, the mean value of three measurements for each side was calculated. Left and right sides values were pooled for subsequent analyses [10]. P value 0.05 was considered significant.

3.1 Descriptive statistics and analysis of the differences between CLBP and asymptomatic groups in the studied conditions

There were no significant between-group differences in the demographic characteristics of the subjects. In this study, surface electromyography and force data of 46 subjects were recorded. There was noise in the force plate signals of six subjects; therefore, the data of these six subjects were excluded. Table 1 illustrates the statistics and between-group analyses of the studied variables for any five conditions. Furthermore, Table 2 lists the P values calculated using the independent t -test to compare the differences between the asymptomatic and CLBP groups. As shown in Table 1, some studied variables significantly deferred between the groups ( p ⩽ 0.05).

Table 2 provides the P values calculated using paired t -test to compare the dependent variables for the studied conditions in each group. In addition, this table lists the P values calculated using the independent t -test to investigate the differences between the CLBP and asymptomatic subjects in terms of the motor and postural strategies in the studied conditions ( p ⩽ 0.05).

4.1 The effects of loading familiarization on neuromuscular responses during SULL in CLBP patients

In the LBP patients, less electrical activity in the TrA/IO and ES muscles in the LL condition and less electrical activity and longer onset latency in the TrA/IO muscle in the RLL were observed. As shown in Table 2, in the LBP subjects, less electrical activity of the ES and EOA muscles were observed in the RLL condition than that in the LL condition. This decrease in the muscle activity may be interpreted as less stiffening or preparatory muscle activity in the trunk muscles or a compensatory (inhibition) mechanism by the CNS to minimize the stress on the lumbar tissues in these patients [32, 33]. These alterations in the trunk muscle activity may cause lower back injuries due to micro trauma. The decrease in muscle activity in the study is consistent with the reports of Sihvonen et al. who showed decreased electrical muscle activity during functional movements in LBP patients [34]. In contrast, this finding contradicts the findings of D’hooge et al. who showed increased electrical activity of the ES muscles with and without load [35].

Moreover, the greater TrA/IO latency in the patients in RLL condition suggests that learning mechanisms may be disturbed in the patients and that they cannot regulate their responses following familiarization of loading.

Alterations in motor control are sometimes interpreted in the context of the pain-spasm-pain model, according to which, pain results in increased muscle activity, resulting in increased pain. In contrast, as per the pain adaptation model, pain decreases muscle activity during muscle activation as an agonist and increases muscle activity during muscle activation as an antagonist [32]. During flexor type SULL on the spine, only the decreased electrical activity of the TrA/IO in the LBP group is consistent with the pain adaptation model [32].

Moreover, in LBP subjects, less IEMG of the EO muscle was observed in the RHL condition than in the unexpected heavy loading (UHL) condition. Longer and shorter peak latencies of the TrA/IO and ES muscles, respectively, were observed in the RHL condition than in the UHL condition. Moreover, compared to the UHL condition, the RHL condition produced a higher increase in the latency of the EO muscle in the LBP subjects than in the asymptomatic subjects.

As the above findings show, before familiarization to heavy loading, the EO muscle showed greater electrical activity in the LBP patients. This may be interpreted as an overestimation in these patients. In addition, in these patients, familiarization shortened the peak latency of the ES muscle and lengthened the peak latency of the TrA/IO muscle. This may be interpreted as a CNS strategy to counteract the flexor moment produced by this type of loading. A higher increase in the latency of the EO muscle in the LBP subjects than in the asymptomatic subjects following familiarization may be interpreted as a wrong modulation of the motor responses in the patients.

4.2 The effects of loading weight on neuromuscular responses during SULL in CLBP patients

In the LBP subjects, shorter latency of the TrA/IO muscle was observed in the RHL condition compared to that in the RLL condition. Crisis in providing stability in the lumbar spine during heavier loading may be a reason for the shorter latency of the TrA/IO muscle.

In addition, compared to the RLL condition, the RHL condition produced a greater increase in the latency of the EO muscle in asymptomatic subjects than in LBP subjects. This may be indicative of the normal response of the neuromuscular system in increasing the latency of the EO muscle following heavier flexor type loading to postpone the more flexor moment. These findings are consistent with those reported by Elizabeth et al., according to which, there were changes in the muscle activity following movement demand changes. Shorter latency of the TrA/IO muscle in the present study may be interpreted as attempt of the CNS to accelerate co contraction of the trunk muscles and provide stiffness and spinal stability. The activities of the transversus abdominis and internal oblique muscles significantly affected IAP and lumbar stability [32].

4.3 The effects of loading size on the neuromuscular responses during SULL in CLBP patients

Moreover, in the asymptomatic subjects, more IEMG and longer peak latency of the ES muscle were found in the HLL condition than in the RHL condition. The findings of the present study are consistent with those of Alearts et al. who reported that corticomotor excitability in the primary motor cortex (M1) is modulated according to the force requirements of the observed grasping and lifting actions [33]. Force requirements of the observed action during movement observation, is a modulating factor in corticomotor excitability of the observer’s primary motor cortex (M1). Lifting heavy objects induces higher M1-excitability than lifting light objects. These findings may support the motor simulation hypothesis, explaining the activation of the motor systems to predict or infer the weight of the lifted object [34].

When lifting objects of identical mass but different sizes, individuals perceived the smaller objects as being heavier than the larger ones (the ‘size-weight’ illusion, SWI). Differences in the mismatch between the actual sensory information and the expected sensory information would induce differences in the apparent weight of each stimulus. It has been demonstrated that individuals are unable to fully scale the load force to the actual mass of the SWI-inducing cubes. Establishing perceptual judgments or interacting with the world highlights are two effective factors for information processing strategies [35].

It is believed that cues from the observed kinematic profile are more effective than the object cues on the encoding of force in the observer’s motor system. The sensory and motor systems are interrelated. The parietal node, namely the inferior parietal lobule (IPL), is assumed to provide a ‘goal-description’ of the observed action, while the frontal part, namely the inferior frontal gyrus (IFG), is suggested to represent the kinematic features of the observed actions. In fact, during action execution, the IFG provides a significant input to M1 and a similar ‘parallel’ IFG-M1 circuit is hypothesized to be recruited [34].

5.1 Study limitation

We noted that there are several potential limitations of this study. Firstly, the experiment was performed on participants with nonspecific low back pain and cannot be generalized for other groups of low back pain patients. Secondly, we did not measure muscle strength, proprioception or flexibility being the possible factors related to the observed differences between asymptomatic and symptomatic participants. Thirdly, this study was conducted among a special age range. The physician and physical therapist should be carefully considered before applying the results to other groups of patients.