Cervical flexion relaxation phenomenon in patients with and without non-specific chronic neck pain

Abstract

BACKGROUND:

The cervical flexion relaxation phenomenon (FRP) is a myoelectric silence of neck extensor muscles which occurs after a certain degree of flexion. Impaired flexion relaxation can impose the vertebral structures to excessive loading resulting from the persistence of muscular contraction.

OBJECTIVE:

This study aimed to investigate the incidence or absence of FRP in cervical erector spinae (CES) and upper trapezius muscles in patients with chronic neck pain (CNP).

METHODS:

Twenty-five patients with CNP and 25 healthy volunteers were recruited. They accomplished cervical flexion and extension from a neutral position in four phases in the sitting position. The surface electromyography activity of both CES and upper trapezius muscles was recorded in each phase. Cervical flexion and extension movements were simultaneously measured using an electrogoniometer.

RESULTS:

FRP in CES was observed in 84% and 36% of healthy subjects and CNP patients, respectively. Flexion relaxation ratio (FRR) in CES was lower in CNP patients than in healthy subjects (mean diff $=$ 1.33; 95% CI: 0.75–1.91) ( $P<$ 0.001). Only in CNP patients, FRR in right erector spinea was significantly higher than that in the left erector spinea ( $P=$ 0.04).

CONCLUSIONS:

FRP incidence in CNP patients was less than in healthy subjects. Moreover, this phenomenon begins later in CNP patients than in healthy subjects indicating prolonged activity of CES muscles during flexion in the CNP group. The difference between FRR in the right and left sides of erector spinea muscles can result in CNP.

Keywords

Flexion relaxation phenomenon chronic neck pain cervical erector spinea

1. Introduction

Chronic neck pain (CNP) is one of the most important musculoskeletal disorders, affecting up to 30–50% of the adult population [1]. CNP can lead to disability and impose an economic burden [2]. Although, in some cases, the potential cause of pain is clear (e.g., infection, fracture, herniated disc), in most cases, the underlying cause of pain is unclear; thus, it is labeled as non-specific chronic neck pain (NSCNP) [3]. Impaired muscle activation patterns, such as deep neck flexor and extensor muscles, were indicated in patients with CNP [4].

Altered muscle activation can be assessed via an abnormal flexion relaxation phenomenon [5]. Flexion relaxation phenomenon (FRP) was first explained by Floyd and Silver as a myoelectric silence of cervical erector spinae (CES) muscles which occur after a certain degree of flexion [6]. Impaired flexion relaxation can impose the vertebral structures to excessive loading resulting from the persistence of muscular contraction. This may result in pain and decreased range of motion and functioning. One of the phenomena of this mechanism is transferring the extension moment from superficial muscles to passive structures of spine. We aimed to transfer the extension moment from the superficial layer of the paraspinae muscles to deeper layers [7, 8, 9].

Murphy et al.’s flexion relaxation ratio (FRR) is an objective assessment method and a reliable marker for neuromuscular impairment which can discriminate CNP patients from healthy subjects [5]. Some studies examined FRP in cervical spinae in healthy subjects. For the first time, Meyer et al. in 1993 examined FRP in cervical erector spinae muscles of 10 asymptomatic individuals. They showed that FRP occurred in 100% of asymptomatic subjects [10]. Moreover, the effect of some factors such as working with the computer, fatigue, speed of movement, and loading of cervical region, trunk positioning, shoulder position, and static neck flexion on FRP was examined in other studies [7, 11, 12, 13, 14, 15]. However, there are few reliable evidences about FRP in patients with chronic neck pain. Airaksinen et al. reported the absence of FRP in a single CNP patient [16]. They visually observed FRP and calculated neither FRR nor the onset/offset angles of FRP. DeVocht et al. calculated FRR in 5 CNP patients and 5 healthy subjects in different positions. They evaluated EMG signals from sternocleidomastoid muscles in the sitting position and in axial rotation movement and reported a significant difference between two groups in terms of FRR [17].

Although there are few evidences to suggest that FRP is somehow different in patients with chronic neck pain, not all characteristics of this phenomenon are clear. A recent study measured the asymmetry of FRR between the right and left sides of erectorspinea muscles in both patients with chronic low back pain and controls. The authors reported that FRR asymmetry in these muscles is significantly more prevalent among patients than healthy subjects. Furthermore, they suggested that an imbalance spine loading could result in low back pain [18]. Asymmetric FRR might cause asymmetric loads on the cervical spinae during flexion and may lead to unilateral over-activity of CES and induce neck pain. To the best of our knowledge, in contrast to low back pain, there is no study that assesses FRP asymmetry between the right and left sides of CES muscles. The comparison of FRP parameters between healthy subjects and NSCNP patients helps us to better understand changes in neuromuscular function in NSCNP patients and helps to choose appropriate interventions to improve it. Therefore, this study aimed at: (1) Determining the incidence or absence of cervical FRP, (2) Calculating the onset/offset angles of FRP, FRR, relaxation time ratio (RTR), (RTR is the percentage of relaxation phase at which EMG silence of CES muscles occurs), (3) Comparing all parameters between NSCNP patients and healthy subjects, and (4) Characterizing the asymmetry of these parameters between the right and left sides of erectorspinea muscles in each group.

2. Methods

2.1 Participants

In this study, taking into account a 15% mean difference in FRR for bilateral erector spinae between two groups as well as $\alpha$ -level of 0.05 (type I error) and $\beta$ -value of 0.20 (type II error), 25 patients with NSCNP and 25 healthy volunteers were recruited. Participants were recruited from September 2019 to February 2020 through a call to orthopedic clinics in Tehran, Iran. Patients were first examined by an orthopedist and included in the study if they were diagnosed with non-specific chronic neck pain. The healthy subjects included students and staff at medical universities. This study was performed in the Biomechanics Laboratory of the Faculty of Rehabilitation Sciences, Shahid Beheshti University of Medical Sciences in Tehran, Iran.

The patient group (12 females and 13 males) was matched with the control group in age, sex, and BMI (frequency matching). A professional physiotherapist with eight years of clinical experience was involved in evaluating the patients and supervising the experiment protocols. The data were extracted from collected EMG signals by another physiotherapist blinded to the subjects’ grouping. The patients were included if they had persistent pain which lasted at least for three months without any specific pathology (e.g., no history of degenerative disease, discopathy, radiculopathy). The patients were excluded if they currently had a pain score more than 50 mm based on the visual analog scale (VAS), systemic disease, cervical or shoulder trauma, or participated in neck muscle strengthening exercises in the past three months. The healthy subjects had no experience of the neck, head, shoulder, or low back pain, at least within the last year. All procedures performed in the study followed the ethical standards of research committee of the School of Rehabilitation, Shahid Beheshti University of Medical Sciences (approval no. IR.SBMU.RETECH.REC.1398.405). All steps of the study were clearly explained to the subjects and they provided written informed consent prior to the start of the study.

2.2 Experimental protocol

During the test, each subject was asked to sit on an adjustable stool with hips and knees at a 90 ${}^{\circ}$ angle, with feet on the floor positioned shoulder-width apart, with arms relaxed by their side, looking at a point that had been located at the eye level. Because variant seated posture can influence cervical spinae posture [19], the subjects were asked to maintain neutral lumbar lordosis and neutral neck posture. Neutral lordosis was regarded as the midpoint between full flexion and extension [20, 21] and was determined by an experienced physiotherapist. Therefore, seated posture was standardized because of neutral lumbar lordosis. Furthermore, each subject was asked to accomplish neck full flexion and extension, and the mid-position was considered neutral neck posture [15, 21]. Moreover, the upper thorax was stabilized by a belt to immobilize this region. Then, the subjects were asked to maintain a neutral starting position for four seconds (phase 1), perform cervical full forward flexion for four seconds (phase 2), maintain full flexion for four seconds (phase 3), and perform re-extension to starting position for four seconds (phase 4) [15]. The protocol of the test was performed in three trials. To control the effects of speed and cumulative daily lauding on FRP parameters, a digital metronome was used, and all subjects performed the test protocol in the morning. Using an electrogoniometer, SEMG signals were recorded bilaterally from the upper trapezius and cervical erector spinae muscles simultaneously during the test. An experienced physiotherapist performed all parts of the protocol.

2.3 Instrumentation

In each trial, EMG signals were recorded by the SEMG device (Datalog, UK). Bipolar disposal EMG surface electrodes (Ag–AgCl) were applied to the skin in the line of muscle fibers. An inter-electrode distance of 2 cm was chosen, and electrode leads were taped on the skin [21, 22]. SEMG data (with a sampling rate of 1,000 Hz and a bandpass filter of 20–480 Hz) were obtained from the right and left CES muscles with a distance of 2 cm lateral to the spinous process c4 [23, 24]. Moreover, to record EMG signals from the left and right upper trapezius muscles, an imaginary line was considered from the C7 spinous process. The posterior part of acromion and the electrodes were placed 20 mm lateral from the line’s midway point [24]. To decrease skin impedance, it was shaved, abraded, and washed using water before placing the electrodes. A ground electrode was applied to the left wrist. Neck flexion and extension angles were recorded via an electrogoniometer sensor (sampling rate of 1000 Hz, Biometrics) synchronized with EMG data.

2.4 Data analysis

Raw EMG data were collected and filtered. The root mean square (RMS) with a 50 ms window of raw EMG (EMG ${}_{\text{RMS}}$ ) was employed to calculate electrical muscle activity amplitude. The EMGRMS provided us with rectified and smoother signals and is a feasible tool for indirectly measuring the strength of muscular activity. The FRR values were obtained by dividing the maximum EMG ${}_{\text{RMS}}$ in the re-extension phase by average EMG ${}_{\text{RMS}}$ in the relaxation phase [14]. Inverse FRR $\leqslant$ 40% was used to judge the existence of FRP [15]. 10% of maximum EMG in re-extension phase was considered a threshold [25, 26], and a flexion angle at which EMG crossed the threshold level to lower values was determined as the onset angle of FRP. A re-extension angle larger than the threshold was determined as the offset angle of FRP. The onset and cessation angles were determined by a synchronized electrogoniometer and were normalized to each subject’s maximum cervical flexion range of motion. RTR was another variable calculated because of the percentage of cervical full flexion phase at which EMG silence occurred.

2.5 Statistical analysis

The distribution of quantitative variables among the healthy subjects and the NSCNP patients was compared using the $t$ -test. The comparisons between the right and left sides of CES in each group were carried out by paired $t$ -test. Furthermore, frequency data were analyzed using the chi-square test. Data were analyzed in Stata software (version 14) and for all statistical tests $p<$ 0.05 was statistically considered significant.

3. Results

The mean age of the 50 subjects was 31.64 $\pm$ 4.98 years (ranging from 23 to 43 years). 54% [27] of the subjects were male (12 subjects in healthy group and 15 subjects in CNP patients). The mean BMI in the subjects was 23.77 $\pm$ 1.66 kg/m ${}^{2}$ (23.86 kg/m ${}^{2}$ in healthy subjects and 23.68 kg/m ${}^{2}$ in CNP patients). The demographics, duration of pain, and a visual analog scale score of participants are shown in Table 1.

Table 1
Distribution of age, weight, BMI, duration of pain and VAS among healthy subjects and non-specific CNP patients

Variable	Healthy ( $n=$ 25)	NSCNP ( $n=$ 25)	$P$ -value ${}^{\ast}$
	Mean (SD)	Mean (SD)
Age (year)	30.64 (4.40)	32.64 (5.41)	0.15
Weight (kg)	69.96 (6.87)	69.64 (4.79)	0.84
BMI (kg/m ${}^{2}$ )	23.86 (1.6)	23.68 (1.75)	0.71
	Median (Q1-Q3)	Median (Q1-Q3)
Duration of pain (month)	–	12 (8–14)	–
VAS (mm)	–	30 (25–30)	–

${}^{*}$ Based on $t$ -test; BMI $=$ Body Mass Index; VAS $=$ Visual Analog Scale; Q1-Q3 $=$ lower and upper quartiles.

FRR for bilateral erector spinea (BE) was lower in the patients with NSCNP than in the healthy subjects and the difference was statistically significant (mean diff $=$ 1.33; 95% CI: 0.75–1.91) ( $P<$ 0.001). However, there was no significant difference between two groups in terms of FRR for bilateral, right and left trapezius (Table 2). Moreover, age and gender had no significant association with FRR ( $P=$ 0.12). FRR in the right erector spinea (RE) was higher than that in the left erector spinea (LE) among healthy subjects (mean diff $=$ 0.98; 95% CI: 0.5–1.46) and NSCNP patients (mean diff $=$ 1.36; 95% CI: 0.91–1.81); it was statistically significant only in non-specific CNP patients ( $P=$ 0.04) (Fig. 1). The frequency of inverse FRR for BE among healthy subjects was higher than that among NSCNP patients (84% vs. 36%) ( $P=$ 0.001) (Fig. 2).

Table 2

Distribution of FRR for trapezious and erector spinae among healthy subjects and non-specific CNP patients

Variable	Healthy ( $n=$ 25)	NSCNP ( $n=$ 25)	$P$ -value ${}^{\ast}$
	Mean (SD)	Mean (SD)
FRR_T	1.64 (0.37)	1.55 (0.13)	0.28
FRR_RT	1.66 (0.39)	1.54 (0.13)	0.15
FRR_LT	1.61 (0.4)	1.5 (0.25)	0.28
FRR_E	3.7 (1.03)	2.37 (0.68)	$<$ 0.001
FRR_RE	3.9 (1.46)	2.43 (0.49)	$<$ 0.001
FRR_LE	3.88 (1.22)	2.42 (0.57)	$<$ 0.001

${}^{*}$ Based on $t$ -test; FRR $=$ Flexion-relaxation ratio; T $=$ Bilateral trapezious; RT $=$ Right trapezious; LT $=$ Left trapezious; E $=$ Bilateral erector spinae; RE $=$ Right erector spinae; LE $=$ Left erector spinae.

Figure 1.

Comparison of flexion-relaxation ratio (FRR) on the right and left side among healthy subjects and non-specific CNP patients.

Figure 2.

Frequency of inverse flexion-relaxation ratio among healthy subjects and non-specific CNP patients.

Figure 3.

Comparison of range of motion among healthy subjects and non-specific CNP patients.

Figure 4.

Comparison of cervical erector spinae onset/offset angles of FRP on the right and left side among healthy subjects and non-specific CNP patients.

The cervical flexion range of motion was significantly different between two groups, and ROM was lower in NSCNP patients (27.67 ${}^{\circ}$ ) than in healthy subjects (38.02 ${}^{\circ}$ ) (Fig. 3). FRP was absent in upper trapezius muscles in both groups. The onset angle of FRP in cervical erector spinae muscles was significantly delayed in the patients compared with healthy group ( $P<$ 0.001). Moreover, there was no significant difference between the right and left sides of CES in each group in terms of the onset/offset angles of FRP ( $P>$ 0.05) (Fig. 4). The results of the paired $t$ -test showed that RTR was significantly higher in healthy subjects (100%) than in NSCNP patients (36%) ( $P<$ 0.001).

4. Discussion

This study showed that FRP occurred only in CES muscles in most of the healthy subjects. This phenomenon was absent in upper trapezius muscles in both the healthy and patient groups. Prolonged flexed postures and altered neuromuscular function can lead to neck pain [12, 27]. Thus, the examination of cervical muscle function during flexion movement plays an important role in assessing the patients with neck pain. Previous study suggested that FRP was a reliable and objective method to examine the altered neuromuscular function [5].

In our study, FRP occurred in 92% of healthy subjects in CES muscles. Similar studies showed that from 95–100% of healthy subjects indicated FRP signs [10, 13, 16]. On the other hand, Burnett et al. showed that FRP occurred in 0–65% of the asymptomatic control group [21].

In the present study, only 25% of NSCNP patients indicated FRP signs. Our findings confirmed the results of the study by Maroufi et al. As they reported, CNP patients had a disability in relaxing their extensor cervical muscles during the flexion movement. Moreover, FRP was not observed in the subjects’ upper trapezius muscles in neither the healthy or patient groups [26].

In this study, the majority of NSCNP patients did not show FRP signs. In other words, pain-induced alteration motor control strategies led to the reduction or elimination of CES muscles’ relaxation time, and these muscles were active through the flexion movement. This alteration in motor control may be a strategy to compensate for the passive system’s lack of stability or caused by insufficient deep cervical flexors. Hence, it may cause the formation of a defective cycle to produce pain and disability [26].

In the present study, a significant difference was observed in FRR between the right and left sides of CES muscles only in NSCNP patients. Asymmetric FRR can not only cause asymmetric loads on the cervical spinae during flexion, but can also lead to unilateral over-activity of CES. In contrast to low back pain, there is no study assessing the asymmetry of FRR in NSCNP. A recent study reported that patients with low back pain indicated FRR asymmetry in their trunk muscles. Furthermore, they reported that FRR asymmetry could induce pain through loading the spine incorrectly due to imbalance muscle activation [28].

The incidence of asymmetric FRR in NSCNP patients is a kind of altered motor control. Altered motor control can lead to the insufficient control of intervertebral joint movements, increased neutral zone, repeated microtrauma, and finally pain [29]. Pain can lead to the alteration in descending drive from supraspinal centers [30]. Moreover, the reflex inhibition of a motor neuron that innervates the painful agonist muscle, is compensated by reorganizing antagonist or synergists muscles; it maintains constant motor output and allows performing the task in the same way under a painless condition [31]. Thus, the pain can both result in altering motor control strategies and subsequent outcomes. Asymmetric FRR can thus both result in and result from NSCNP.

FRR in CES muscles in NSCNP patients was lower than that in healthy subjects. However, there was no significant difference in upper trapezius muscles between two groups. A decrease in FRR can result from either increased muscle activity in the relaxation phase or reduced muscle activity in the re-extension phase. In the study by Maroufi et al., the magnitude of CES muscle activity in CNP patients in all phases of the flexion movement was higher than that in healthy group [26]. Therefore, the increased myoelectric activity of CES muscles in the relaxation phase in NSCNP patients decreases FRR.

The onset/offset angles were calculated to determine FRP duration. In the present study, FRP was started sooner and ended equally in healthy subjects compared with NSCNP patients. Despite the lack of studies about the determination of FRP’s onset/offset angles in the NSCNP patients, some studies measured these angles in healthy subjects. Mousavi et al. reported that FRP started in 68% of full flexion which ended in 95% of full flexion in healthy subjects [15]. Moreover, Pialasse et al. showed that FRP in healthy subjects started in 75% of full flexion which ended in 92% of full flexion [13]. Douglas et al. showed that FRP started in 85% of full flexion in CES muscles in healthy subjects. They did not calculate the offset angle of FRP [32]. In our study, FRP appeared in 75% of full flexion and disappeared in 94% of full flexion in healthy subjects, consistent to the results of previous studies.

In the present study, the onset angle of FRP in CES muscles increased in the patients compared with the healthy subjects. There was no statistically significant difference between the two groups in terms of the offset angle; this finding is not in line with the results of previous study. Panjabi’s model of stability can explain it; pain-induced inhibition of deep cervical muscles and insufficient control of passive system resulted in a decrease in cervical stability. Thus, superficial muscles have to work a long time to provide cervical stability. It was estimated that this angle increase may be a protective strategy to provide stability and prevent injury. Moreover, considering the fear-avoidance model, pain-related fear of movement can cause the maladaptive changes in the neuromuscular system to prevent further injury [33]. Because to this model, NSCNP patients may be unable to relax their neck muscles and increase FRP’s onset angle.

Mousavi et al. showed that the augmentation of these angles may be caused by creep development of passive structures after static flexion, the decrease in cervical stability, and long-time compensatory activity of superficial muscles to provide enough stability [15]. On the other hand, Zabihhossenian et al. showed that neck muscle fatigue leads to the decreased onset and offset angles. They reported that fatigued muscles are more likely to become unable to provide cervical stability, leading to the earlier onset and later offset angles of FRP following fatigue which might be attributed to transfer loads from superficial cervical muscles to deep muscles and passive structures during full flexion movement [12].

RTR was calculated as a percentage of the relaxation phase at which EMG silence of CER muscles occurs. In the present study, RTR decreased in the patient group, as compared with the healthy subjects. The decline of RTR can be attributed to three mechanisms: 1) late onset of CES muscles to start flexion; 2) disability of CES muscles to relax during full flexion; 3) early onset of CES muscles during the re-extension phase. Our study ruled out the last mechanism because there was no statistical difference between the two groups in terms of the offset angle in the present study. It was estimated that these mechanisms are essential to provide cervical stability and prevent injury. Our study showed that cervical ROM in the NSCNP patients group decreased, as compared with the healthy subjects. This may be caused by both prolonged activity and disability in relaxing CES muscles which confirmed the altered motor control in these patients to provide enough stability.

The results of this study could not be generalized to all patients with chronic neck pain, in particular the findings about FRR asymmetry, because patients with VAS scores $>$ 50 were excluded from the study. Further studies are necessary to evaluate the effect of pain intensity on flexion-relaxation parameters in patients with chronic neck pain.

Since it was difficult to record the myoelectric activity of deep muscles, it was necessary to measure CES muscles activity’s magnitude to get better information about FRP. Analysis of normalized SEMG of CES combined with FRP parameters can give more information about CES muscles’ neuromuscular function in the NSCNP patients and the healthy subjects. Future studies must also focus on rehabilitation protocols such as stability exercise on FRP in NSCNP patients.

5. Conclusion

This study showed that FRP was more prevalent among healthy subjects than CNP patients. The onset of FRP and RTR in NSCNP patients decreased, as compared with the healthy subjects. Moreover, asymmetric FRR between the right and left sides of erector spinea muscles can result in CNP. CES muscles’ prolonged activity to provide the stability of the cervical spinae is considered to be responsible for the decrease in these parameters in the NSCNP patients. FRR in CES muscles in the NSCNP patients decreased, as compared with the healthy subjects, because of the overactivity of these muscles in the relaxation phase.

Footnotes

Acknowledgments

This paper was extracted from a physiotherapy graduate thesis. The authors would like to express our gratitude to all staff of the School of Rehabilitation, Iran as well as to all individuals who helped us complete this research project.

Conflict of interest

None to report.

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Cervical flexion relaxation phenomenon in patients with and without non-specific chronic neck pain

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1. Introduction

2. Methods

2.1 Participants

2.2 Experimental protocol

2.3 Instrumentation

2.4 Data analysis

2.5 Statistical analysis

3. Results

Table 1 Distribution of age, weight, BMI, duration of pain and VAS among healthy subjects and non-specific CNP patients

5. Conclusion

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Distribution of age, weight, BMI, duration of pain and VAS among healthy subjects and non-specific CNP patients