Introduction

Cervicogenic headache (CGH) is one of the most common types of headache affecting about 2.5% of the general population and also observed more frequently among middle-aged patients especially in women; in addition, 17.8% of people complain about frequent headaches [ 1 ].

The cervical spine is considered a referral site for the pain experienced by CGH patients, considered chronic and manifested as unilateral cephalgia that may be developed due to musculoskeletal problems in the neck. Pain is transferred from the cervical spine to the face and then to the head by sensory fibers in the upper three cervical spinal nerves when converged with the trigeminal nerve located at the trigeminocervical nucleus. The spinal accessory nerve is assumed to affect by this pain referral mechanism. Accordingly, before reaching the descending tract of the trigeminal nerve, spinal accessory nerve fibers are connected to the nerve roots of the upper cervical spine [ 1 - 3 ].

Elastic modulus is an indicator of the stiffness of the tissue, used as an index for showing the number of attached cross-bridges [ 4 ]. Cervical pain in CGH can lead to increased neutrally mediated reflex stiffness in cervical muscles by influencing alpha-motor neurons. Enhanced stimulation of these neurons can increase the frequency of attached cross-bridges in the actin and myosin filaments of these muscles [ 5 ].

According to the muscle mechanics theory, the intensity of stiffness in a joint partly depends on the internal spring-like stiffness of the muscles attached to that joint [ 6 ], i.e. increased stiffness of cervical muscle can reduce the range of motion (ROM) in the cervical region in CGH patients [ 7 ].

Thus, based on the mechanism of CGH, some authors have proposed increased stiffness of neck muscles and restricted cervical ROM as clinical characteristics of CGH [ 1 , 8 , 9 ].

Forward head posture (FHP) is excessive anterior positioning of the head compared to a vertical reference line [ 10 ]. Quek et al. showed that higher FHP correlated with more deficits in cervical ROM and confirmed that treating FHP can lead to improving cervical impairments [ 11 ]. Cervical impairment and ROM limitation are proposed as characteristics of CGH. Therefore, FHP may be a prevalent abnormal posture among CGH patients, causing or aggravating CGH [ 12 ]. Watson et al. found that FHP is more common in CGH patients than normal subjects [ 13 ]. However, Zito et al. showed that FHP is not a prevalent abnormal posture among CGH patients [ 14 ].

Although stiffness of neck muscles, limited cervical ROM, and FHP are proposed as clinical characteristics of CGH [ 1 , 8 , 9 , 12 ], only one study (Park et al.) addressed the elastic modulus of neck muscles in CGH patients [ 15 ]. Moreover, previous studies on cervical ROM [ 16 - 19 ] and FHP in CGH patients have reported controversial results. Thus, this study aimed to compare the elastic modulus of suboccipital muscles, cervical ROM, and FHP in CGH and normal subjects.

Material and Methods

In this cross-sectional study, data were collected from 20 CGH patients (15 females and 5 males) and the same number of healthy individuals (14 females, 6 males). The two groups were matched in terms of age, height, weight, and body mass index (BMI). The participant’s basic characteristics are shown in the results. CGH patients were selected according to ICHD-2018 criteria for diagnosis of CGH (e.g., Spurling’s test in the cervical region leading to headache in these patients). All participants received some information about the objectives, the procedures, and the data collection process was ensured that their identity and information would remain anonymous and signed informed consent to enter the study. This study was conducted based on a research protocol confirmed by the Ethical Committee of Tarbiat Modares University.

Basic evaluation

Elastic modulus of suboccipital muscles was measured based on elastic modulus equals stress/strain (Hooke’s law of elasticity) [ 20 , 21 ].

Based on the studies, applying compressive force and detecting changes in ultrasound images can be effective for evaluating biomechanical properties of the tissues such as stiffness [ 22 , 23 ]. Accordingly, in the present study, the following method was used for measuring elastic modulus:

The subject lay prone and a transducer of sonography apparatus (Siemens Medical Solutions, USA) was placed in the first segment of cervical vertebrae next to the spinous process. To gain elastic modulus, compressive force (F) was applied to the transducer and the images were recorded in two force levels (F1=0N and F2=2N). The strain was determined by measuring the diameter of suboccipital muscles at two force levels (L1 and L2) using image J software according to the equation Strain = (L2-L1)/L1. Stress was determined based on the applied force (F) measured with a force gauge connected to the transducer via a retaining ring made of polylactic acid, according to the equation Stress = F2-F1/S (the area of the transducer) [ 22 , 23 ].

Previous studies have confirmed the reliability of assessment of mechanical properties of muscles using ultrasonography [ 24 , 25 ] that is the basis of elastography (ultrasonography signals before and after a distorting force to form an image of the tissue’s response by comparing the two signals [ 26 ]), whose reliability and validity have been approved by previous studies [ 27 - 30 ]. Moreover, the method used in the present study is widely applied to diagnose malignancies in the liver, prostate, breast, cervix, thyroid, pancreas, and lymph nodes based on the elastic modulus in the tissue. Considering biomechanical variations in neuromuscular and musculoskeletal problems, the technique used in the present study can have clinical applications in musculoskeletal problems [ 22 ].

Neck ROM was measured by the universal goniometer (UG), whose reliability has been confirmed by previous studies [ 31 - 33 ]. The cervical ROM measurement was done in a standardized sitting position to eliminate errors and prevent improper movements. The participants were required to sit with their back straightly closed to the back of the chair. The reference points for the placement of UG were determined according to the method proposed by Youdas et al., [ 33 ]. To measure flexion and extension, the UG axis was held on the tragus of the ear so that the movable arm was parallel with the base of the nares and the fixed arm was vertical. For side flexion, the UG axis was held on a sternal notch, the stationary arm tracked an imaginary line running from the participant’s acromion processes and the movable arm was along the center of the person’s nose. For rotation, the axis of UG was placed above the midpoint of the participant’s head. The fixed arm of UG followed an imaginary line between the person’s acromion processes, while the movable arm was placed along the tip of the person’s nose.

FHP was assessed using two methods as follows:

1) Measuring craniovertebral angle (CVA) using a digital imaging technique. The markers used for specifying the landmarks were fixed to C7 (detected by palpation and after excluding C6) and the easily identified tragus of the ear. Lateral photographs were taken from the subjects in the standing posture. The CVA was identified using the image taken from a digital camera at the meeting point of a horizontal line crossing the C7 spinous process and another line connecting the midpoint of the tragus to the skin on the top of the C7 spinous process. In addition, CVA was measured by Image J software whose reliability and validity were confirmed [ 34 ]. Measurement of CVA for FHP assessment has been validated in the literature [ 35 , 36 ].

2) Measuring the distance between the anterior tragus of the ear and the vertical line passed from the anterior lateral malleolus in the sagittal plane according to the Kendall and Mccreary method [ 37 ].

Statistical analysis

The data in this study were processed with SPSS-26 software and the CGH and control groups were statistically compared using the Mann–Whitney U test. Statistical significant level was considered at P<0.05.

Results

Independent T-Test showed that there is no significant differences between the participant’s basic characteristics (Table 1).

The elastic modulus of suboccipital muscles in the members of the CGH group was greater than that in the individuals in the normal group, showing a significant difference (P=0.008) (Table 2). FHP showed no significant intergroup difference, but ROM of cervical extension (P=0.035), right rotation (P=0.046), and left rotation (P=0.018) were significantly reduced in the CGH group compared to the normal group (Table 2).

Discussion

In this study, the elastic modulus was used as an indicator of the stiffness of suboccipital muscles that stiffness in muscles was used as an index showing the number of attached cross-bridges [ 4 ]. According to previous studies, cervical pain in CGH can increase the number of attached cross-bridges of the actin and myosin filaments and cause spasm and increased stiffness in cervical muscles [ 5 ]. Thus, some authors have proposed increased stiffness of neck muscles as a clinical characteristic of CGH [ 1 , 8 , 9 ].

In this study, measuring the elastic modulus of suboccipital muscles showed that they were significantly stiffer in the CGH patients than in normal healthy subjects. In the literature, only one study assessed the elastic modulus of these muscles [ 15 ], which its findings supported the results obtained from the present study.

Different methods were used to measure the elastic modulus of tissues: the measuring procedure used by Park et al. involved pressing an oscillatory device against the skin with a force of 0.18 N and an instant impulse of 0.4 N for 15 milliseconds. The skin surface oscillation induced by this device was estimated to verify the value of the mechanical variability [ 15 ]. Other devices used to measure the elastic modulus were durometer [ 38 ] and shear wave elastography [ 39 ]. Although all of these systems were reliable for qualitative assessment and diagnosis of diseases, various quantitative analysis methods are utilized for computing stiffness in these devices. For example, however, shear wave elastography measures the propagation speed of the shear wave, the durometer uses resistance to indentation for stiffness analysis. On the other hand, the resolution is different in these elastography devices. Therefore, the method and device used for measuring the elastic modulus can affect the results, and thus methodological differences should be noticed when comparing the results of different studies [ 40 ].

Suboccipital muscles in CGH patients seem stiffer than those in healthy subjects. However, this conclusion needs attesting by more studies with consistent methods of measuring elastic modulus and larger samples.

This study showed that cervical pain increases the stiffness of suboccipital muscles, leading to dysfunction in CGH patients. In this study, therefore, cervical ROM in these patients was assumed to be limited in comparison with normal subjects. Generally, it is proposed that, in chronic pain syndromes, the pain reduces the ROM of painful parts [ 41 ]. The findings of this study confirmed this result and showed that ROM of cervical extension (P=0.035), right rotation (P=0.046), and left rotation (P=0.018) in CGH patients were significantly smaller than that in normal subjects. Based on the results of Zwart’s study, the patients with CGH were significantly different from healthy normal subjects in terms of rotation (P<0.001) and flexion/extension (P<0.001), but not in terms of lateral neck movement [ 17 ]. Zito et al. showed that CGH patients had a lower cervical range of flexion/extension in comparison with the normal group [ 18 ]. Further, Jull et al. reported that active cervical ROM (extension and bilateral rotation) in patients with CGH was significantly different from that of the patients suffering from migraine and tension-type headache and asymptomatic controls [ 1 ]. Huber et al. reported that all cervical movements (especially flexion) decreased in CGH patients [ 1 ]. However, Hall et al. found no difference between patients with CGH and the normal group in terms of active cervical ROM [ 19 ] that their results may have been affected by compensatory movements of other spinal levels. It was presumed that the most limited cervical movements in CGH patients are rotation and extension, but further researches are needed to confirm this conclusion.

Both the Kendall and McCreary method and CVA measurement in this study showed that the FHP variable was not significantly different between CGH patients and normal subjects.

Watson and Trott concluded that FHP was more common in CGH patients compared to other patients [ 14 ]. More recently, however, Zito et al. found no significant differences in the prevalence of FHP in CGH or migraine patients in comparison with normal ones [ 14 ]. Farmer et al. reported no significant difference in posture between the CGH patients and normal subjects [ 12 ].

Different factors can be considered for neck pain in CGH patients and FHP is considered age-related, leading to CGH in older subjects, and the other factors are more common in younger patients [ 18 ]. Further researches are needed to compare the FHP of CGH patients in different age groups. However, based on two methods in this study, assessing FHP and confirming the results of this study by most recent studies, FHP cannot be used as a diagnostic criterion for CGH. Thus, although FHP may be related to a decrease in cervical ROM, it is not the prevalent posture in CGH patients and its modification should not be considered as a major and general treatment for CGH.

Conclusion

According to the data in this study, suboccipital muscles in CGH patients were stiffer and ROM of cervical rotation and extension were smaller in these patients than in the normal group, resulting in diagnosing the CGH and treatment. However, FHP is not the most common posture in CGH patients, this posture cannot be used as a diagnostic criterion for CGH and its modification should not be considered as a major and general treatment for CGH. Further studies should be conducted on larger samples to measure stiffness in CGH patients and compare the results with the data obtained in the present study.

Acknowledgment

The authors would like to thank all the people who eagerly participated in the current study.

Authors’ Contribution

F. Bahrpeyma was the supervisor of the project and conceived the original idea. M. Tavakkoli carried out the study and wrote the manuscript. Both of authors read, modified, and approved the final version of the manuscript.

Ethical Approval

This study was conducted based on a research protocol confirmed by the Ethical Committee of Tarbiat Modares University with the code IR.modares.REC.1397.238.

Informed Consent

All participants received some information about the objectives, the procedures, and the data collection process was ensured that their identity and information would remain anonymous and signed informed consent to enter the study.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of Interest

None

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