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Phys. Ther. Korea 2022; 29(3): 180-186

Published online August 20, 2022

https://doi.org/10.12674/ptk.2022.29.3.180

© Korean Research Society of Physical Therapy

Comparison of Muscle Thickness and Changing Ratio for Cervical Flexor Muscles During the Craniocervical Flexion Test Between Subjects With and Without Forward Head Posture

Jae-hyun Lee1 , PT, BPT, Ui-jae Hwang2,3 , PT, PhD, Oh-yun Kwon2,3 , PT, PhD

1Department of Physical Therapy, The Graduate School, Yonsei University, 2Kinetic Ergocise Based on Movement Analysis Laboratory, 3Department of Physical Therapy, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju, Korea

Correspondence to: Oh-yun Kwon
E-mail: kwonoy@yonsei.ac.kr
https://orcid.org/0000-0002-9699-768X

Received: April 14, 2022; Revised: April 29, 2022; Accepted: May 4, 2022

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Background: The craniocervical flexion test (CCFT) was developed for the activation and endurance of deep cervical flexors. However, the muscle thickness and muscle thickness changing ratio of the sternocleidomastoid (SCM) and deep cervical flexor (DCF) muscles in subjects with and without forward head posture (FHP) have not been reported. Objects: To determine the difference in thickness of the SCM and DCF muscles and the difference in the muscle thickness changing ratio between SCM, DCF, and DCF/SCM 20 mmHg and DCF/SCM 30 mmHg between subjects with and without FHP.
Methods: Thirty subjects with and without FHP were enrolled. The muscle thickness of the SCM and DCF was measured when maintained at a baseline pressure of 20 mmHg and a maximum pressure of 30 mmHg using a pressure biofeedback unit during the CCFT. Ultrasonography was used to capture images of SCM and DCF muscle thickness during the CCFT, which was calculated using the picture archiving and communication system (PACS).
Results: We observed a significant difference within the pressure main effect between SCM and DCF at a baseline pressure of 20 mmHg and a maximum pressure of 30 mmHg (p < 0.05). However, there was no significant difference in the muscle thickness and muscle thickness changing ratio for SCM and DCF during CCFT between subjects with and without FHP.
Conclusion: There was no significant difference in the muscle thickness recruitment pattern during CCFT in posture changes between subjects with and without FHP.

Keywords: Neck muscles, Posture, Ultrasonography

Forward head posture (FHP) refers to the forward protrusion of the head with respect to the body based on the vertical posture line of the human body [1]. The FHP is the most common type of abnormal head posture and is defined when the upper cervical vertebrae (C1-C3) are extended and the lower cervical vertebrae (C4-C7) are identified as flexed [2,3]. An increase in FHP due to abnormal posture is associated with lengthening of the upper cervical flexor muscles, such as the longus colli (LCo) and longus capitis (LC), and the lengthening of the lower cervical extensor muscles, such as the semispinalis cervicis; C6/7-C2, T1-C4, and T1-C5 superficial multifidus; C5/6-C3 and C6/7-C4 deep multifidus; and splenius cervicis [4,5]. In addition, increased FHP is associated with shortening of the upper cervical extensor muscles, such as the rectus capitis posterior minor and major, the obliquus capitis superior, and the semispinalis capitis, as well as shortening of the lower cervical flexor muscles, such as the sternocleidomastoid (SCM) and anterior and middle scalene [4,5]. FHP is characterized by poor body alignment and typical muscle imbalances and is a perpetuating factor in chronic neck pain [6].

The craniocervical flexion test (CCFT) is a strategy to activate the deep cervical flexor (DCF) muscles, such as the LCo and LC, and perform endurance through movements of the upper cervical flexion [7]. Subjects with neck pain have been shown to have higher muscle activity in the SCM and anterior scalene during the CCFT than healthy subjects [7,8]. The SCM has upper cervical extension and lower cervical flexion moment arms, while the LCo and LC have upper cervical and lower cervical flexion moment arms [9]. In the CCFT, patients should perform craniocervical flexion and increase DCF activation, but those with neck pain show compensatory actions, such as neck retraction and increase SCM activation [7].

Ultrasonography can measure muscle thickness, muscle fiber pennation, and muscle fiber length under static and dynamic conditions [10,11]. Ultrasound is a safe, non-invasive method that can measure changes in the thickness of superficial and deep muscles without crosstalk from adjacent muscles [10-12]. Ultrasonography has a high correlation with magnetic resonance imaging (MRI) (intraclass correlation coefficients, ICC = 0.78 to 0.95), and its validity has been proven for measuring muscle thickness [13].

The CCFT has been used to test DCF activation and endurance by gradually increasing the pressure by 2 mmHg from a baseline of 20 mmHg to a maximum of 30 mmHg [7]. In a previous study, the electromyography (EMG) amplitude of the DCF muscles was positively correlated with the incremental stages during the CCFT [14]. Jesus et al. [10] reported that healthy subjects showed a progressive increase in SCM and DCF muscle thickness when the stage of the pressure biofeedback unit (PBU) was increased during the CCFT. However, subjects with neck pain show overactivation of the superficial cervical flexor muscles such as the SCM and AS during CCF due to impaired DCF activation [7,15]. This suggests that subjects with neck pain use an altered muscle strategy of the superficial and deep cervical flexors (DCFs) to perform the CCFT [15].

The craniocervical flexion exercises is a low-load training program that trains from a baseline pressure of 20 mmHg to a maximum pressure of 30 mmHg without the dominant use of superficial muscles [16]. A previous study reported that individuals with FHP demonstrated significantly increased SCM thickness compared to those without FHP during the CCFT [17]. The changes in muscle thickness are correlated with amplitude of the EMG signal [18]. This means that more change in muscle thickness express more muscle EMG activity, and quantifying muscle thickness changes may indirectly represent muscle function [18,19]. However, no studies have compared the muscle thickness and muscle thickness changing ratio for the SCM and DCF muscles when performing the CCFT between subjects with and without FHP. Therefore, the purpose of this study was to compare the muscle thickness and muscle thickness changing ratio of the SCM, DCF, and DCF/SCM during CCFT in subjects with and without FHP. We hypothesized that subjects with FHP would demonstrate greater muscle thickness and muscle thickness changing ratio in the SCM and less muscle thickness and muscle thickness changing ratio in the DCF.

1. Subjects

This study was conducted at Wonju H Hospital. In total, 30 healthy subjects aged 20–40 years with and without FHP were recruited (with FHP = 15, without FHP = 15). Subjects with FHP were defined as those with a craniovertebral angle (CVA) of < 50° [20]. The characteristics of the participants are shown in Table 1. The inclusion criteria were subjects without neck pain who could understand the purpose of the study and perform CCFT. The exclusion criteria were a history of fractures in the neck and shoulder region, non-structural abnormalities of the spine, and neck or shoulder pain. The research protocol was approved by the Institutional Review Board of Yonsei University (IRB no. 1041849-202109-BM-141-01). The study process was explained to all the subjects prior to the study, and all subjects signed an informed consent form.

Table 1 . Characteristics of the subjects (N = 30).

VariableWith FHP (n=15)Without FHP (n=15)p-value
Age (y)28.0 ± 5.030.1 ± 3.00.467
Height (cm)162.3 ± 29.1168.1 ± 9.00.186
Weight (kg)73.7 ± 16.964.1 ± 13.80.097
CV angle45.6 ± 3.353.9 ± 1.90.001*

Values are presented as mean ± standard deviation. FHP, forward head posture; CV angle, cranio-vertebral angle. *Significant difference (p < 0.05)..



2. Instrumentation

1) Craniovertebral angle

The CVA was measured between the horizontal line drawn by the skin overlying the C7 spinous process and a line joining the midpoint of the tragus of the ear [17,21]. An adhesive reflex marker was attached to the spinous process of C7 [21]. To evaluate the posture of the standing subject’s neck and head, a digital camera (Samsung Galaxy A9, Samsung, Seoul, Korea) was set perpendicular to the ground and pointed directly at the lateral aspect of the subject’s shoulder 1.5-m away to minimize parallax error [2,21,22]. Next, the principal investigator asked the subject to flex and extend their neck three times, with the front of the face assuming a natural posture [2]. The CVA was measured using a digital camera, and ImageJ imaging analysis software (National Institutes of Health, Bethesda, MD, USA) was used to calculate the CVA.

2) Ultrasonography

Ultrasonography was used to capture SCM and DCF muscle images from a baseline pressure of 20 mmHg to a maximum pressure of 30 mmHg during CCFT [10]. A 7.5-MHz transducer was placed longitudinally parallel to the right trachea, approximately 5-cm from the midline. In this position, the ultrasonography image allowed proper visualization of the SCM, DCF, right carotid artery, vertebral lamina, and SCM boundary (benchmark). Contraction of the SCM and DCF was identified, and the clearest screen was captured and saved [10,17]. The thicknesses of the SCM and DCF were calculated after transmitting the image to a picture archiving and communication system (PACS) and a medical image storage and transmission system. The muscle thickness was calculated from the superficial to deep boundaries of the SCM. The DCF muscle thickness was calculated from the inferior border of the carotid boundary to the superior border of the echogenic vertebral laminae [10,17]. The average value was calculated by making three lines at 1, 2, and 3 cm from the middle of the measurement image to the right (Figure 1). The muscle thickness changing ratio during CCFT was expressed as the ratio of muscle thickness change to muscle thickness at a baseline pressure of 20 mmHg [10]. The muscle thickness changing ratio of the SCM, DCF, DCF/SCM 20 mmHg, and DCF/SCM 30 mmHg were calculated as follows: 1) SCM thickness changing ratio- SCM 30 mmHg/SCM 20 mmHg, 2) DCF thickness changing ratio- DCF 30 mmHg/DCF 20 mmHg, 3) DCF/SCM thickness changing ratio 20 mmHg- DCF 20 mmHg/SCM 20 mmHg, and 4) DCF/SCM thickness changing ratio 30 mmHg- DCF 30 mmHg/SCM 30 mmHg. In this study, we measured muscle thickness changing ratio for SCM 30 mmHg/SCM 20 mmHg, DCF 30 mmHg/DCF 20 mmHg, DCF/SCM 20 mmHg, and DCF/SCM 30 mmHg between subjects with and without FHP. The muscle thickness changing ratio of SCM, DCF, and DCF/SCM can be used as a valuable measurement to compare muscle performance at a baseline pressure of 20 mmHg and maximum pressure of 30 mmHg between subjects with and without FHP.

Figure 1. Ultrasonography image. SCM, sternocleidomastoid; DCF, deep cervical flexor.

3. Experimental Procedure

The subject assumed a hook-lying position with flexion of the hip at 45° and knee at 90° in the supine position. The PBU unit was placed behind the upper cervical region and inflated to a baseline pressure of 20 mmHg by the principal investigator (Figure 2). The principal investigator asked the subjects to perform an upper cervical flexion movement from a baseline pressure of 20 mmHg to a maximum pressure of 30 mmHg during the CCFT. Preliminary practice was conducted to control the subject’s craniocervical flexion speed and posture. Craniocervical flexion contraction was maintained for 10 seconds when a baseline pressure of 20 mmHg to a maximum pressure of 30 mmHg was reached [7,10,14].

Figure 2. (A) Pressure biofeedback unit. (B) Measurement set-up.

4. Statistical Analysis

The Kolmogorov–Smirnov Z-test was used to verify the normality of the data. Two-way repeated-measures analysis of variance (ANOVA) was applied to identify significant differences between groups (with and without FHP) and within pressure (20 mmHg and 30 mmHg) in the muscle thickness and muscle thickness changing ratio of SCM, DCF, and DCF/SCM. Two-way repeated-measure ANOVA was conducted to compare the muscle thickness changing ratio for baseline pressure of 20 mmHg and maximum pressure of 30 mmHg between groups with and without FHP, as well as the interaction effect (pressure x groups). When statistically significant differences were found, an independent t-test was used to determine between-group differences, and a paired t-test was used to determine within-pressure differences. Additionally, an independent t-test was used for comparison between groups of each muscle contraction ratio, such as SCM 30mmHg/SCM 20mmHg and DCF 30mmHg/DCF 20mmHg. All statistical analyses were performed using SPSS software (ver. 18.0; IBM Co., Armonk, NY, USA). The averages and standard deviations were calculated for all variables. Statistical significance was set at p < 0.05.

A statistically significant difference main effect was observed in the muscle thickness of the SCM and DCF within pressure (20 and 30 mmHg). In subjects with and without FHP demonstrated progressive increase in the muscle thickness of SCM and DCF with increasing pressure at a baseline pressure of 20 mmHg to maximum pressure of 30 mmHg during CCFT (Tables 2, 3). However, there were no significant differences between the groups (Tables 2, 3). In the Table 4, there were no significant difference between groups for SCM 30 mmHg/SCM 20 mmHg and DCF 30 mmHg/DCF 20 mmHg. Additionally, there were no significant main or interaction effects on the muscle thickness changing ratio for the DCF/SCM 20 mmHg and DCF/SCM 30 mmHg (Table 5).

Table 2 . Within (20 and 30 mmHg) and between (with and without FHP) differences in muscle thickness of the SCM (cm).

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg0.76 ± 0.140.79 ± 0.170.001*0.7160.899
30 mmHg0.89 ± 0.220.91 ± 0.24

Values are presented as mean ± standard deviation. FHP, forward head posture; SCM, sternocleidomastoid. *Significant difference (p < 0.05)..


Table 3 . Within (20 and 30 mmHg) and between (with and without FHP) differences in muscle thickness of the DCF (cm).

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg1.23 ± 0.241.26 ± 0.320.001*0.9510.273
30 mmHg1.37 ± 0.261.34 ± 0.38

Values are presented as mean ± standard deviation. FHP, forward head posture; DCF, deep cervical flexor. *Significant difference (p < 0.05)..


Table 4 . Comparison of the muscle thickness changing ratio for SCM 30/20 mmHg and DCF 30/20 mmHg between subjects with and without FHP.

PressureWith FHP (n=15)Without FHP (n=15)tp-value
SCM 30/20 mmHg1.17 ± 0.221.17 ± 0.250.050.96
DCF 30/20 mmHg1.12 ± 0.111.07 ± 0.131.260.22

Values are presented as mean ± standard deviation. SCM, sternocleidomastoid; DCF, deep cervical flexor; FHP, forward head posture..


Table 5 . Within (DCF/SCM 20 mmHg and DCF/SCM 30 mmHg) and between (with and without FHP) differences in muscle thickness changing ratio.

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg1.66 ± 0.441.64 ± 0.410.1440.7320.637
30 mmHg1.60 ± 0.391.52 ± 0.40

Values are presented as mean ± standard deviation. DCF, deep cervical flexor; SCM, sternocleidomastoid; FHP, forward head posture..


The present study compared the muscle thickness and muscle thickness changing ratio for the SCM and DCF during the CCFT between subjects with and without FHP. We hypothesized that during the CCFT, the participants with an FHP would show greater muscle thickness and muscle thickness changing ratio of the SCM. However, the results showed no significant difference in the muscle thickness of the SCM and DCF between subjects with and without FHP. Additionally, there was no significant difference in the muscle thickness changing ratio of the SCM 30 mmHg/SCM 20 mmHg, DCF 30 mmHg/DCF 20 mmHg, DCF/SCM 20 mmHg, and DCF/SCM 30 mmHg.

FHP progressively shortens the anterior scalene and SCM due to excessive head protrusion in the vertical reference line [23]. In addition, when the suboccipital muscles are shortened due to FHP, the length of the DCF muscles increases, and the length-tension curve changes require more torque from the LCo and LC during craniocervical flexion [24]. Changes in the length-tension curve result in “stretch weakness” [25]. The CCFT is a satisfactory clinical method for evaluating the performance of the LC in synergy with the LCo [26]. As the CCFT pressure increases, the muscle recruitment patterns of the SCM and DCF are measured using ultrasonography [10]. In this study, the muscle thickness of the SCM and DCF increased as the CCFT pressure increased between subjects with and without FHP, but there was no significant difference between the groups in the muscle thickness and muscle thickness changing ratio for SCM and DCF.

In this study, there was no significant difference in the DCF muscle thickness and DCF muscle thickness changing ratio at a baseline pressure of 20 mmHg and a maximal pressure of 30 mmHg between subjects with and without FHP. In a previous study, the DCF thickness was shown to be reduced in subjects with FHP compared to those without FHP [27]. In a previous study, the muscle thickness of the LCo in the resting state, contraction state (50% of maximal isometric contraction of craniocervical flexion), and thickness change between subjects with and without FHP were measured using ultrasonography [19]. Participants performed craniocervical flexion movements while push on the inferior load cell placed on their chin in a sitting position [19]. The results of a previous study showed greater muscle thickness change of LCo during craniocervical flexion in subjects without FHP compared subjects with FHP [19]. This can be explained by the fact that the FHP translated forward in relation to a vertical reference line [2,22,27], as well as the disuse of the DCF muscles in daily living and overuse of the SCM muscle in neck flexion movements [19]. For SCM, there was no significant difference in the SCM muscle thickness and muscle thickness changing ratio between subjects with and without FHP. Previous studies have argued the importance of the initial head position of the CCFT in minimizing superficial muscle activity in subjects with FHP [17]. When the forehead and chin of the subject with FHP are on the horizontal line, the DCF is shortened, and the SCM is overactivated during the CCFT [17].

Our results of the CCFT showed no significant difference in the muscle thickness and muscle thickness changing ratio for SCM and DCF between subjects with and without FHP. The possible reasons for this observation are as follows: 1) Previous studies recruited subjects with moderate FHP (CVA < 43.2°) [17], but we recruited subjects with a slight degree of FHP (CVA < 49.1°) [21], which may explain the lack of significance at a baseline pressure of 20 mmHg and maximum pressure of 30 mmHg. 2) We did not recruit participants with neck pain. Previous studies do not support the relationship between sagittal neck posture in a sitting posture and neck pain [28]. Additionally, FHP was significantly correlated with the neck pain scale in adults and older adults, and adults with neck pain showed increased FHP compared with asymptomatic adults [29]. In this study, as the CCFT was performed in healthy subjects without neck pain, it is thought that posture did not affect the craniocervical flexion movement pattern. 3) In this study, the muscle thickness of the SCM and DCF increased with increasing pressure during the CCFT. Low-load craniocervical flexion exercises can effectively train DCFs [7], but patients with neck pain show high EMG amplitudes in the SCM and AS [16]. Rehabilitation of patients with neck pain requires effective training through low-load craniocervical flexion exercises to increase DCF muscle activation and decrease SCM muscle activation [16]. This low-load exercise is considered necessary for coordination between the deep and superficial flexors in patients with neck pain [16]. 4) Finally, It would have been difficult to accurately detect muscle thickness using ultrasonography compared to EMG amplitudes that detect the superficial and DCF muscles. Therefore, it is possible that there is no significant difference in SCM thickness between subjects with and without FHP.

Ultrasound is useful as a clinical evaluation tool because it can show changes in muscle thickness through real-time feedback [10,11] and allow for muscle thickness change measurement between SCM and DCF during the CCFT [10]. A previous study argued that mechanical compression of the surrounding muscles reduces the thickness of the DCF during CCFT because the DCF muscle has a smaller cross-sectional area than the superficial cervical flexor muscles [10]. Changes in muscle thickness measured using ultrasonography can help detect muscle contraction patterns [19]. However, the reliability of a noninvasive and objective assessment of the muscle thickness recruitment patterns of the SCM and DCF measured by ultrasonography would be requires further study [10].

The present study has some limitations. First, the study subjects consisted of healthy adults in their 20s and 30s. Therefore, the results cannot be generalized to the overall population. Second, as we did not recruit subjects with neck pain, the results cannot be generalized to this population. Third, CVA does not represent the shape of the cervical spine radiology [30]. Therefore, subject evaluation between subjects with and without FHP according to the CVA needs to be improved.

Our results confirmed that there was no significant difference in muscle thickness for SCM and DCF or muscle thickness changing ratio for SCM 30 mmHg/SCM 20 mmHg, DCF 30 mmHg/DCF 20 mmHg, DCF/SCM 20 mmHg, and DCF/SCM 30 mmHg during the CCFT between subjects with and without FHP. Significant differences were demonstrated only with progressive increase in the SCM and DCF muscle thickness with increasing at a baseline pressure of 20 mmHg to maximum pressure of 30 mmHg. However, there was no significant difference in the muscle thickness recruitment pattern between subjects with and without FHP. It is considered that the difference in CVA does not necessarily affect the craniocervical flexion movement pattern between the subjects with and without FHP. Therefore, postural changes due to slight differences in CVA between subjects with and without FHP require monitoring to improve muscle recruitment patterns during CCFT.

No potential conflicts of interest relevant to this article are reported.

Conceptualization: JL, UH, OK. Data curation: JL. Formal analysis: JL, UH, OK. Investigation: JL. Methodology: JL, UH, OK. Project administration: JL, UH, OK. Supervision: JL, UH, OK. Validation: UH, OK. Visualization: JL. Writing - original draft: JL, UH. Writing - review & editing: JL, OK.

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Article

Original Article

Phys. Ther. Korea 2022; 29(3): 180-186

Published online August 20, 2022 https://doi.org/10.12674/ptk.2022.29.3.180

Copyright © Korean Research Society of Physical Therapy.

Comparison of Muscle Thickness and Changing Ratio for Cervical Flexor Muscles During the Craniocervical Flexion Test Between Subjects With and Without Forward Head Posture

Jae-hyun Lee1 , PT, BPT, Ui-jae Hwang2,3 , PT, PhD, Oh-yun Kwon2,3 , PT, PhD

1Department of Physical Therapy, The Graduate School, Yonsei University, 2Kinetic Ergocise Based on Movement Analysis Laboratory, 3Department of Physical Therapy, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju, Korea

Correspondence to:Oh-yun Kwon
E-mail: kwonoy@yonsei.ac.kr
https://orcid.org/0000-0002-9699-768X

Received: April 14, 2022; Revised: April 29, 2022; Accepted: May 4, 2022

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background: The craniocervical flexion test (CCFT) was developed for the activation and endurance of deep cervical flexors. However, the muscle thickness and muscle thickness changing ratio of the sternocleidomastoid (SCM) and deep cervical flexor (DCF) muscles in subjects with and without forward head posture (FHP) have not been reported. Objects: To determine the difference in thickness of the SCM and DCF muscles and the difference in the muscle thickness changing ratio between SCM, DCF, and DCF/SCM 20 mmHg and DCF/SCM 30 mmHg between subjects with and without FHP.
Methods: Thirty subjects with and without FHP were enrolled. The muscle thickness of the SCM and DCF was measured when maintained at a baseline pressure of 20 mmHg and a maximum pressure of 30 mmHg using a pressure biofeedback unit during the CCFT. Ultrasonography was used to capture images of SCM and DCF muscle thickness during the CCFT, which was calculated using the picture archiving and communication system (PACS).
Results: We observed a significant difference within the pressure main effect between SCM and DCF at a baseline pressure of 20 mmHg and a maximum pressure of 30 mmHg (p < 0.05). However, there was no significant difference in the muscle thickness and muscle thickness changing ratio for SCM and DCF during CCFT between subjects with and without FHP.
Conclusion: There was no significant difference in the muscle thickness recruitment pattern during CCFT in posture changes between subjects with and without FHP.

Keywords: Neck muscles, Posture, Ultrasonography

INTRODUCTION

Forward head posture (FHP) refers to the forward protrusion of the head with respect to the body based on the vertical posture line of the human body [1]. The FHP is the most common type of abnormal head posture and is defined when the upper cervical vertebrae (C1-C3) are extended and the lower cervical vertebrae (C4-C7) are identified as flexed [2,3]. An increase in FHP due to abnormal posture is associated with lengthening of the upper cervical flexor muscles, such as the longus colli (LCo) and longus capitis (LC), and the lengthening of the lower cervical extensor muscles, such as the semispinalis cervicis; C6/7-C2, T1-C4, and T1-C5 superficial multifidus; C5/6-C3 and C6/7-C4 deep multifidus; and splenius cervicis [4,5]. In addition, increased FHP is associated with shortening of the upper cervical extensor muscles, such as the rectus capitis posterior minor and major, the obliquus capitis superior, and the semispinalis capitis, as well as shortening of the lower cervical flexor muscles, such as the sternocleidomastoid (SCM) and anterior and middle scalene [4,5]. FHP is characterized by poor body alignment and typical muscle imbalances and is a perpetuating factor in chronic neck pain [6].

The craniocervical flexion test (CCFT) is a strategy to activate the deep cervical flexor (DCF) muscles, such as the LCo and LC, and perform endurance through movements of the upper cervical flexion [7]. Subjects with neck pain have been shown to have higher muscle activity in the SCM and anterior scalene during the CCFT than healthy subjects [7,8]. The SCM has upper cervical extension and lower cervical flexion moment arms, while the LCo and LC have upper cervical and lower cervical flexion moment arms [9]. In the CCFT, patients should perform craniocervical flexion and increase DCF activation, but those with neck pain show compensatory actions, such as neck retraction and increase SCM activation [7].

Ultrasonography can measure muscle thickness, muscle fiber pennation, and muscle fiber length under static and dynamic conditions [10,11]. Ultrasound is a safe, non-invasive method that can measure changes in the thickness of superficial and deep muscles without crosstalk from adjacent muscles [10-12]. Ultrasonography has a high correlation with magnetic resonance imaging (MRI) (intraclass correlation coefficients, ICC = 0.78 to 0.95), and its validity has been proven for measuring muscle thickness [13].

The CCFT has been used to test DCF activation and endurance by gradually increasing the pressure by 2 mmHg from a baseline of 20 mmHg to a maximum of 30 mmHg [7]. In a previous study, the electromyography (EMG) amplitude of the DCF muscles was positively correlated with the incremental stages during the CCFT [14]. Jesus et al. [10] reported that healthy subjects showed a progressive increase in SCM and DCF muscle thickness when the stage of the pressure biofeedback unit (PBU) was increased during the CCFT. However, subjects with neck pain show overactivation of the superficial cervical flexor muscles such as the SCM and AS during CCF due to impaired DCF activation [7,15]. This suggests that subjects with neck pain use an altered muscle strategy of the superficial and deep cervical flexors (DCFs) to perform the CCFT [15].

The craniocervical flexion exercises is a low-load training program that trains from a baseline pressure of 20 mmHg to a maximum pressure of 30 mmHg without the dominant use of superficial muscles [16]. A previous study reported that individuals with FHP demonstrated significantly increased SCM thickness compared to those without FHP during the CCFT [17]. The changes in muscle thickness are correlated with amplitude of the EMG signal [18]. This means that more change in muscle thickness express more muscle EMG activity, and quantifying muscle thickness changes may indirectly represent muscle function [18,19]. However, no studies have compared the muscle thickness and muscle thickness changing ratio for the SCM and DCF muscles when performing the CCFT between subjects with and without FHP. Therefore, the purpose of this study was to compare the muscle thickness and muscle thickness changing ratio of the SCM, DCF, and DCF/SCM during CCFT in subjects with and without FHP. We hypothesized that subjects with FHP would demonstrate greater muscle thickness and muscle thickness changing ratio in the SCM and less muscle thickness and muscle thickness changing ratio in the DCF.

MATERIALS AND METHODS

1. Subjects

This study was conducted at Wonju H Hospital. In total, 30 healthy subjects aged 20–40 years with and without FHP were recruited (with FHP = 15, without FHP = 15). Subjects with FHP were defined as those with a craniovertebral angle (CVA) of < 50° [20]. The characteristics of the participants are shown in Table 1. The inclusion criteria were subjects without neck pain who could understand the purpose of the study and perform CCFT. The exclusion criteria were a history of fractures in the neck and shoulder region, non-structural abnormalities of the spine, and neck or shoulder pain. The research protocol was approved by the Institutional Review Board of Yonsei University (IRB no. 1041849-202109-BM-141-01). The study process was explained to all the subjects prior to the study, and all subjects signed an informed consent form.

Table 1 . Characteristics of the subjects (N = 30).

VariableWith FHP (n=15)Without FHP (n=15)p-value
Age (y)28.0 ± 5.030.1 ± 3.00.467
Height (cm)162.3 ± 29.1168.1 ± 9.00.186
Weight (kg)73.7 ± 16.964.1 ± 13.80.097
CV angle45.6 ± 3.353.9 ± 1.90.001*

Values are presented as mean ± standard deviation. FHP, forward head posture; CV angle, cranio-vertebral angle. *Significant difference (p < 0.05)..



2. Instrumentation

1) Craniovertebral angle

The CVA was measured between the horizontal line drawn by the skin overlying the C7 spinous process and a line joining the midpoint of the tragus of the ear [17,21]. An adhesive reflex marker was attached to the spinous process of C7 [21]. To evaluate the posture of the standing subject’s neck and head, a digital camera (Samsung Galaxy A9, Samsung, Seoul, Korea) was set perpendicular to the ground and pointed directly at the lateral aspect of the subject’s shoulder 1.5-m away to minimize parallax error [2,21,22]. Next, the principal investigator asked the subject to flex and extend their neck three times, with the front of the face assuming a natural posture [2]. The CVA was measured using a digital camera, and ImageJ imaging analysis software (National Institutes of Health, Bethesda, MD, USA) was used to calculate the CVA.

2) Ultrasonography

Ultrasonography was used to capture SCM and DCF muscle images from a baseline pressure of 20 mmHg to a maximum pressure of 30 mmHg during CCFT [10]. A 7.5-MHz transducer was placed longitudinally parallel to the right trachea, approximately 5-cm from the midline. In this position, the ultrasonography image allowed proper visualization of the SCM, DCF, right carotid artery, vertebral lamina, and SCM boundary (benchmark). Contraction of the SCM and DCF was identified, and the clearest screen was captured and saved [10,17]. The thicknesses of the SCM and DCF were calculated after transmitting the image to a picture archiving and communication system (PACS) and a medical image storage and transmission system. The muscle thickness was calculated from the superficial to deep boundaries of the SCM. The DCF muscle thickness was calculated from the inferior border of the carotid boundary to the superior border of the echogenic vertebral laminae [10,17]. The average value was calculated by making three lines at 1, 2, and 3 cm from the middle of the measurement image to the right (Figure 1). The muscle thickness changing ratio during CCFT was expressed as the ratio of muscle thickness change to muscle thickness at a baseline pressure of 20 mmHg [10]. The muscle thickness changing ratio of the SCM, DCF, DCF/SCM 20 mmHg, and DCF/SCM 30 mmHg were calculated as follows: 1) SCM thickness changing ratio- SCM 30 mmHg/SCM 20 mmHg, 2) DCF thickness changing ratio- DCF 30 mmHg/DCF 20 mmHg, 3) DCF/SCM thickness changing ratio 20 mmHg- DCF 20 mmHg/SCM 20 mmHg, and 4) DCF/SCM thickness changing ratio 30 mmHg- DCF 30 mmHg/SCM 30 mmHg. In this study, we measured muscle thickness changing ratio for SCM 30 mmHg/SCM 20 mmHg, DCF 30 mmHg/DCF 20 mmHg, DCF/SCM 20 mmHg, and DCF/SCM 30 mmHg between subjects with and without FHP. The muscle thickness changing ratio of SCM, DCF, and DCF/SCM can be used as a valuable measurement to compare muscle performance at a baseline pressure of 20 mmHg and maximum pressure of 30 mmHg between subjects with and without FHP.

Figure 1. Ultrasonography image. SCM, sternocleidomastoid; DCF, deep cervical flexor.

3. Experimental Procedure

The subject assumed a hook-lying position with flexion of the hip at 45° and knee at 90° in the supine position. The PBU unit was placed behind the upper cervical region and inflated to a baseline pressure of 20 mmHg by the principal investigator (Figure 2). The principal investigator asked the subjects to perform an upper cervical flexion movement from a baseline pressure of 20 mmHg to a maximum pressure of 30 mmHg during the CCFT. Preliminary practice was conducted to control the subject’s craniocervical flexion speed and posture. Craniocervical flexion contraction was maintained for 10 seconds when a baseline pressure of 20 mmHg to a maximum pressure of 30 mmHg was reached [7,10,14].

Figure 2. (A) Pressure biofeedback unit. (B) Measurement set-up.

4. Statistical Analysis

The Kolmogorov–Smirnov Z-test was used to verify the normality of the data. Two-way repeated-measures analysis of variance (ANOVA) was applied to identify significant differences between groups (with and without FHP) and within pressure (20 mmHg and 30 mmHg) in the muscle thickness and muscle thickness changing ratio of SCM, DCF, and DCF/SCM. Two-way repeated-measure ANOVA was conducted to compare the muscle thickness changing ratio for baseline pressure of 20 mmHg and maximum pressure of 30 mmHg between groups with and without FHP, as well as the interaction effect (pressure x groups). When statistically significant differences were found, an independent t-test was used to determine between-group differences, and a paired t-test was used to determine within-pressure differences. Additionally, an independent t-test was used for comparison between groups of each muscle contraction ratio, such as SCM 30mmHg/SCM 20mmHg and DCF 30mmHg/DCF 20mmHg. All statistical analyses were performed using SPSS software (ver. 18.0; IBM Co., Armonk, NY, USA). The averages and standard deviations were calculated for all variables. Statistical significance was set at p < 0.05.

RESULTS

A statistically significant difference main effect was observed in the muscle thickness of the SCM and DCF within pressure (20 and 30 mmHg). In subjects with and without FHP demonstrated progressive increase in the muscle thickness of SCM and DCF with increasing pressure at a baseline pressure of 20 mmHg to maximum pressure of 30 mmHg during CCFT (Tables 2, 3). However, there were no significant differences between the groups (Tables 2, 3). In the Table 4, there were no significant difference between groups for SCM 30 mmHg/SCM 20 mmHg and DCF 30 mmHg/DCF 20 mmHg. Additionally, there were no significant main or interaction effects on the muscle thickness changing ratio for the DCF/SCM 20 mmHg and DCF/SCM 30 mmHg (Table 5).

Table 2 . Within (20 and 30 mmHg) and between (with and without FHP) differences in muscle thickness of the SCM (cm).

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg0.76 ± 0.140.79 ± 0.170.001*0.7160.899
30 mmHg0.89 ± 0.220.91 ± 0.24

Values are presented as mean ± standard deviation. FHP, forward head posture; SCM, sternocleidomastoid. *Significant difference (p < 0.05)..


Table 3 . Within (20 and 30 mmHg) and between (with and without FHP) differences in muscle thickness of the DCF (cm).

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg1.23 ± 0.241.26 ± 0.320.001*0.9510.273
30 mmHg1.37 ± 0.261.34 ± 0.38

Values are presented as mean ± standard deviation. FHP, forward head posture; DCF, deep cervical flexor. *Significant difference (p < 0.05)..


Table 4 . Comparison of the muscle thickness changing ratio for SCM 30/20 mmHg and DCF 30/20 mmHg between subjects with and without FHP.

PressureWith FHP (n=15)Without FHP (n=15)tp-value
SCM 30/20 mmHg1.17 ± 0.221.17 ± 0.250.050.96
DCF 30/20 mmHg1.12 ± 0.111.07 ± 0.131.260.22

Values are presented as mean ± standard deviation. SCM, sternocleidomastoid; DCF, deep cervical flexor; FHP, forward head posture..


Table 5 . Within (DCF/SCM 20 mmHg and DCF/SCM 30 mmHg) and between (with and without FHP) differences in muscle thickness changing ratio.

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg1.66 ± 0.441.64 ± 0.410.1440.7320.637
30 mmHg1.60 ± 0.391.52 ± 0.40

Values are presented as mean ± standard deviation. DCF, deep cervical flexor; SCM, sternocleidomastoid; FHP, forward head posture..


DISCUSSION

The present study compared the muscle thickness and muscle thickness changing ratio for the SCM and DCF during the CCFT between subjects with and without FHP. We hypothesized that during the CCFT, the participants with an FHP would show greater muscle thickness and muscle thickness changing ratio of the SCM. However, the results showed no significant difference in the muscle thickness of the SCM and DCF between subjects with and without FHP. Additionally, there was no significant difference in the muscle thickness changing ratio of the SCM 30 mmHg/SCM 20 mmHg, DCF 30 mmHg/DCF 20 mmHg, DCF/SCM 20 mmHg, and DCF/SCM 30 mmHg.

FHP progressively shortens the anterior scalene and SCM due to excessive head protrusion in the vertical reference line [23]. In addition, when the suboccipital muscles are shortened due to FHP, the length of the DCF muscles increases, and the length-tension curve changes require more torque from the LCo and LC during craniocervical flexion [24]. Changes in the length-tension curve result in “stretch weakness” [25]. The CCFT is a satisfactory clinical method for evaluating the performance of the LC in synergy with the LCo [26]. As the CCFT pressure increases, the muscle recruitment patterns of the SCM and DCF are measured using ultrasonography [10]. In this study, the muscle thickness of the SCM and DCF increased as the CCFT pressure increased between subjects with and without FHP, but there was no significant difference between the groups in the muscle thickness and muscle thickness changing ratio for SCM and DCF.

In this study, there was no significant difference in the DCF muscle thickness and DCF muscle thickness changing ratio at a baseline pressure of 20 mmHg and a maximal pressure of 30 mmHg between subjects with and without FHP. In a previous study, the DCF thickness was shown to be reduced in subjects with FHP compared to those without FHP [27]. In a previous study, the muscle thickness of the LCo in the resting state, contraction state (50% of maximal isometric contraction of craniocervical flexion), and thickness change between subjects with and without FHP were measured using ultrasonography [19]. Participants performed craniocervical flexion movements while push on the inferior load cell placed on their chin in a sitting position [19]. The results of a previous study showed greater muscle thickness change of LCo during craniocervical flexion in subjects without FHP compared subjects with FHP [19]. This can be explained by the fact that the FHP translated forward in relation to a vertical reference line [2,22,27], as well as the disuse of the DCF muscles in daily living and overuse of the SCM muscle in neck flexion movements [19]. For SCM, there was no significant difference in the SCM muscle thickness and muscle thickness changing ratio between subjects with and without FHP. Previous studies have argued the importance of the initial head position of the CCFT in minimizing superficial muscle activity in subjects with FHP [17]. When the forehead and chin of the subject with FHP are on the horizontal line, the DCF is shortened, and the SCM is overactivated during the CCFT [17].

Our results of the CCFT showed no significant difference in the muscle thickness and muscle thickness changing ratio for SCM and DCF between subjects with and without FHP. The possible reasons for this observation are as follows: 1) Previous studies recruited subjects with moderate FHP (CVA < 43.2°) [17], but we recruited subjects with a slight degree of FHP (CVA < 49.1°) [21], which may explain the lack of significance at a baseline pressure of 20 mmHg and maximum pressure of 30 mmHg. 2) We did not recruit participants with neck pain. Previous studies do not support the relationship between sagittal neck posture in a sitting posture and neck pain [28]. Additionally, FHP was significantly correlated with the neck pain scale in adults and older adults, and adults with neck pain showed increased FHP compared with asymptomatic adults [29]. In this study, as the CCFT was performed in healthy subjects without neck pain, it is thought that posture did not affect the craniocervical flexion movement pattern. 3) In this study, the muscle thickness of the SCM and DCF increased with increasing pressure during the CCFT. Low-load craniocervical flexion exercises can effectively train DCFs [7], but patients with neck pain show high EMG amplitudes in the SCM and AS [16]. Rehabilitation of patients with neck pain requires effective training through low-load craniocervical flexion exercises to increase DCF muscle activation and decrease SCM muscle activation [16]. This low-load exercise is considered necessary for coordination between the deep and superficial flexors in patients with neck pain [16]. 4) Finally, It would have been difficult to accurately detect muscle thickness using ultrasonography compared to EMG amplitudes that detect the superficial and DCF muscles. Therefore, it is possible that there is no significant difference in SCM thickness between subjects with and without FHP.

Ultrasound is useful as a clinical evaluation tool because it can show changes in muscle thickness through real-time feedback [10,11] and allow for muscle thickness change measurement between SCM and DCF during the CCFT [10]. A previous study argued that mechanical compression of the surrounding muscles reduces the thickness of the DCF during CCFT because the DCF muscle has a smaller cross-sectional area than the superficial cervical flexor muscles [10]. Changes in muscle thickness measured using ultrasonography can help detect muscle contraction patterns [19]. However, the reliability of a noninvasive and objective assessment of the muscle thickness recruitment patterns of the SCM and DCF measured by ultrasonography would be requires further study [10].

The present study has some limitations. First, the study subjects consisted of healthy adults in their 20s and 30s. Therefore, the results cannot be generalized to the overall population. Second, as we did not recruit subjects with neck pain, the results cannot be generalized to this population. Third, CVA does not represent the shape of the cervical spine radiology [30]. Therefore, subject evaluation between subjects with and without FHP according to the CVA needs to be improved.

CONCLUSIONS

Our results confirmed that there was no significant difference in muscle thickness for SCM and DCF or muscle thickness changing ratio for SCM 30 mmHg/SCM 20 mmHg, DCF 30 mmHg/DCF 20 mmHg, DCF/SCM 20 mmHg, and DCF/SCM 30 mmHg during the CCFT between subjects with and without FHP. Significant differences were demonstrated only with progressive increase in the SCM and DCF muscle thickness with increasing at a baseline pressure of 20 mmHg to maximum pressure of 30 mmHg. However, there was no significant difference in the muscle thickness recruitment pattern between subjects with and without FHP. It is considered that the difference in CVA does not necessarily affect the craniocervical flexion movement pattern between the subjects with and without FHP. Therefore, postural changes due to slight differences in CVA between subjects with and without FHP require monitoring to improve muscle recruitment patterns during CCFT.

ACKNOWLEDGEMENTS

None.

FUNDING

None to declare.

CONFLICTS OF INTEREST

No potential conflicts of interest relevant to this article are reported.

AUTHOR CONTRIBUTION

Conceptualization: JL, UH, OK. Data curation: JL. Formal analysis: JL, UH, OK. Investigation: JL. Methodology: JL, UH, OK. Project administration: JL, UH, OK. Supervision: JL, UH, OK. Validation: UH, OK. Visualization: JL. Writing - original draft: JL, UH. Writing - review & editing: JL, OK.

Fig 1.

Figure 1.Ultrasonography image. SCM, sternocleidomastoid; DCF, deep cervical flexor.
Physical Therapy Korea 2022; 29: 180-186https://doi.org/10.12674/ptk.2022.29.3.180

Fig 2.

Figure 2.(A) Pressure biofeedback unit. (B) Measurement set-up.
Physical Therapy Korea 2022; 29: 180-186https://doi.org/10.12674/ptk.2022.29.3.180

Table 1 . Characteristics of the subjects (N = 30).

VariableWith FHP (n=15)Without FHP (n=15)p-value
Age (y)28.0 ± 5.030.1 ± 3.00.467
Height (cm)162.3 ± 29.1168.1 ± 9.00.186
Weight (kg)73.7 ± 16.964.1 ± 13.80.097
CV angle45.6 ± 3.353.9 ± 1.90.001*

Values are presented as mean ± standard deviation. FHP, forward head posture; CV angle, cranio-vertebral angle. *Significant difference (p < 0.05)..


Table 2 . Within (20 and 30 mmHg) and between (with and without FHP) differences in muscle thickness of the SCM (cm).

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg0.76 ± 0.140.79 ± 0.170.001*0.7160.899
30 mmHg0.89 ± 0.220.91 ± 0.24

Values are presented as mean ± standard deviation. FHP, forward head posture; SCM, sternocleidomastoid. *Significant difference (p < 0.05)..


Table 3 . Within (20 and 30 mmHg) and between (with and without FHP) differences in muscle thickness of the DCF (cm).

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg1.23 ± 0.241.26 ± 0.320.001*0.9510.273
30 mmHg1.37 ± 0.261.34 ± 0.38

Values are presented as mean ± standard deviation. FHP, forward head posture; DCF, deep cervical flexor. *Significant difference (p < 0.05)..


Table 4 . Comparison of the muscle thickness changing ratio for SCM 30/20 mmHg and DCF 30/20 mmHg between subjects with and without FHP.

PressureWith FHP (n=15)Without FHP (n=15)tp-value
SCM 30/20 mmHg1.17 ± 0.221.17 ± 0.250.050.96
DCF 30/20 mmHg1.12 ± 0.111.07 ± 0.131.260.22

Values are presented as mean ± standard deviation. SCM, sternocleidomastoid; DCF, deep cervical flexor; FHP, forward head posture..


Table 5 . Within (DCF/SCM 20 mmHg and DCF/SCM 30 mmHg) and between (with and without FHP) differences in muscle thickness changing ratio.

PressureWith FHPWithout FHPWithin-pressure
main effect (p)
Between-group
main effect (p)
Within x between
interaction effect (p)
20 mmHg1.66 ± 0.441.64 ± 0.410.1440.7320.637
30 mmHg1.60 ± 0.391.52 ± 0.40

Values are presented as mean ± standard deviation. DCF, deep cervical flexor; SCM, sternocleidomastoid; FHP, forward head posture..


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