MRI-based assessment paraspinal extensor muscle fatty infiltration in acute cervical spinal cord injury patients - a retrospective study

Abstract

Background

The effect of fat infiltration in the paraspinal muscles on cervical degenerative disease has been confirmed by multiple studies. However, little is known about fat infiltration in the paraspinal extensors in patients with acute cervical spinal cord injury (SCI). This study aimed to investigate the difference in paraspinal extensor fatty infiltration between patients with acute cervical SCI and healthy controls, and to further explore the protective role of the paravertebral extensor muscles in patients with cervical SCI.

Methods

A total of 50 patients with acute cervical SCI admitted to the emergency department from January 2019 to November 2023 were retrospectively analyzed, including 26 males and 24 females, with an average age of 59.60 ± 10.81 years. A control group of 50 healthy middle-aged and elderly individuals was also included, comprising 28 males and 22 females, with an average age of 55.00 ± 8.21 years. Cervical spine magnetic resonance imaging (MRI) was used to measure the cross-sectional areas of the superficial and deep cervical extensor muscles, the corresponding vertebral body cross-sectional areas, and the fat area within the superficial and deep extensor muscle groups using Image J software. Differences between the two groups were compared, and the cervical SCI patients were further analyzed based on the severity of the spinal cord injury and gender differences.

Results

The deep fatty infiltration ratio (DFIR) and superficial fatty infiltration ratio (SFIR) at C4-C7 in the cervical SCI group were significantly higher than those in the control group (P < 0.001). The cross-sectional area of the functional deep extensor area (FDEA) relative to the vertebral body area (VBA) and the cross-sectional area of the functional superficial extensor area (FSEA) relative to the VBA at the C5 and C6 levels in the cervical SCI group were significantly lower than those in the control group (P < 0.001, P < 0.001, P = 0.034, P = 0.004 respectively). Among the cervical SCI patients, the cross-sectional areas of the deep extensor area (DEA) and the superficial extensor area (SEA) in males were significantly higher than those in females (P < 0.001). At the C6 and C7 levels, the FDEA/VBA and FSEA/VBA ratios in the male group were higher than those in the female group (P = 0.009, P = 0.022, P = 0.019, P = 0.005, respectively).

Conclusion

Patients with acute cervical SCI exhibit significantly higher fatty infiltration and a greater degree of paravertebral extensor muscle degeneration compared to healthy controls. This finding underscores the importance of the paravertebral extensor muscles in the context of cervical SCI and may guide future therapeutic strategies.

Introduction

Spinal cord injury (SCI) is increasingly acknowledged as a critical global health concern, particularly within the context of cervical SCI [1]. These injuries typically result from mechanisms such as flexion, hyperextension, compression, shearing, and rotation, often manifesting clinically through a combination of these mechanisms [2]. It is crucial to monitor SCI trends rigorously and identify high-risk populations to effectively implement targeted preventive policies. Recent literature has extensively documented the correlation between paraspinal muscle and fat infiltration and their influence on cervical spine alignment maintenance [3,4,5]. These studies have illuminated the stabilizing and protective functions of paraspinal muscles. They provide essential physical support to the spine and are integral to postural biomechanics, proprioception, and fine motor control [6, 7], prompting growing interest among clinicians. Moreover, multiple investigations have underscored the protective significance of neck muscle strength in various accidental injuries, including traffic accidents, falls from height, slips, and high-impact sports collisions [8, 9]. Currently, extensive evidence exists from numerous studies on the atrophic degeneration of paraspinal muscles in chronic SCI patients, yet research focusing on these muscles in acute cervical SCI patients remains limited. With the increasing clinical use of cervical spine magnetic resonance imaging (MRI), our observations reveal heightened levels of paraspinal muscle fat infiltration in acutely admitted cervical SCI patients during their initial comprehensive MRI scans [10, 11]. This study aims to delineate differences between this cohort and the general population and to explore the protective role of paraspinal muscles in cervical SCI patients. Specifically, we hypothesize that individuals with cervical SCI exhibit increased paraspinal muscle fat infiltration compared to healthy counterparts.

Methods

A retrospective review was conducted on medical records and radiological data of patients treated for acute cervical SCI at the Department of Spine Surgery, Longyan First Hospital, from January 2019 to November 2023. The inclusion and exclusion criteria for this study are shown in the table below (Table 1). The study protocol received approval from our hospital’s Health Scie.

Table 1 The inclusion and exclusion criteria

Assessment of cervical spinal cord injury

In this study, the ASIA classification system was utilized for assessment. ASIA grade A indicates complete injury, characterized by the absence of both motor and sensory functions in the S4-S5 sacral segments. Grade B represents incomplete injury, where there is preservation of some sensory function below the level of injury but complete motor loss. Grade C denotes incomplete injury, with preserved motor function below the injury level, yet more than half of the key muscles have a strength less than grade 3. Grade D signifies incomplete injury, where more than half of the key muscles below the injury level have a strength grade of 3 or higher. Grade E indicates normal motor and sensory functions. Previous studies have suggested a more favorable prognosis for patients classified as ASIA grade D [13]. Therefore, patients classified as grades A, B, or C were grouped as having severe symptomatology, while those classified as grade D were categorized as having mild symptomatology by the authors. In the supplementary material, we have provided three representative images for each ASIA grade (Fig. S1).

Imaging procedures of MRI

In this study, transverse T2-weighted magnetic resonance images were obtained at the level of the vertebral endplates spanning C4-C7 using the Picture Archiving and Communication System (PACS) imaging system for both patient groups. Position with a 3.0TMRI machine (Achieva 3.0 T; Philips Company). There were 12 transaxial slices in each MRI, 3 slices per level, slice thickness 2.5 mm, and spacing 0.25 mm. The sequence of the T2-weighted axial images was 20 × 20 cm field of view, 324 × 252 matrix, 3000 ms repetition time, 110 ms echo time, with 2 excitations.

Cervical muscle measurements

Images were analyzed at the vertebral endplates of C4-C7. Due to the proximity of the C3 vertebra to the attachment points of the deep cervical extensor muscles and suboccipital muscles, measurement errors in muscle cross-sectional area were considered significant and were therefore excluded from the study. The cervical paraspinal muscles were anatomically classified into the deep and superficial layers of the cervical extensor muscle group. The deep layer includes the multifidus, semispinalis cervicis, and levator scapulae muscles, while the superficial layer comprises the splenius capitis, semispinalis capitis, and spinalis cervicis muscles. Measurements in this study were conducted using ImageJ software (National Institutes of Health, Bethesda, MD). These measurements encompassed the cross-sectional area of the deep extensor (DEA), superficial extensor (SEA), and corresponding vertebral body (VBA). The pseudocolor tool in ImageJ was utilized to identify adipose tissue regions, highlighted in red, enabling computation of the fatty area (FA) within the deep and superficial extensor muscle groups. Subtracting the adipose tissue area from the total muscle area yielded the functional deep extensor area (FDEA) and functional superficial extensor area (FSEA), as illustrated in Fig. 1. The ratios of FA to DEA or FA to SEA were calculated to determine the deep fatty infiltration ratio (DFIR) and superficial fatty infiltration ratio (SFIR) of the cervical extensor muscles, respectively. Following previous research [14,15,16,17], the ratios of FDEA to VBA and FSEA to VBA were utilized to standardize muscle area measurements [13], thereby mitigating the influence of variations in patient body size on measurement outcomes. The imaging measurements were independently taken by two experienced spine surgeons as observers, blinded to any patient information and each other’s measurements. Intra-observer and inter-observer reliability were assessed using intra-class correlation coefficients (ICC). The inter-observer agreement ICC was 0.829 [95% CI 0.732–0.889], and the intra-observer ICC were 0.826 [95% CI 0.752–0.879] and 0.838 [95% CI 0.764–0.896].

Fig. 1

Schematic representation of measurements conducted using Image J. Notes: This is a schematic representation of MRI cross-sections of the C4-5 level in SCI and normal patients. (A) The T2-weighted axial MRI images of patients with cervical spinal cord injury were processed using Image J software to apply pseudocolor mapping (ASIA grade D). (B) In the MRI images of patients with cervical spinal cord injury, the vertebral body, deep paraspinal extensors, and superficial paraspinal extensors have been outlined with yellow lines for clear identification. (ASIA grade D). (C) The area of adipose tissue within the demarcated paraspinal muscle regions was calculated using Image J software and is identified with yellow coloration (ASIA grade D). (D) The T2-weighted axial MRI images of normal control group were processed using Image J software to apply pseudocolor mapping (ASIA grade E). (E) Original transverse section of the cervical spine in the normal control group (ASIA grade E). (F) Corresponding paraspinal muscle fat area (highlighted in yellow) in the normal control group (ASIA grade E). ASIA American Spinal Cord Injury Association, DEA indicates cross-sectional area of deep extensors; SEA, cross-sectional area of superficial extensors; VBA, cross-sectional area of the vertebral body

Statistical analysis

Statistical analysis of the acquired data was conducted using SPSS 27.0 software. Data distribution was assessed for normality or approximate normality, and results were expressed as mean ± standard deviation (x̅ ± s). Independent sample t-tests were employed to compare the VBA, DEA, SEA, DFIR, SFIR, FDEA/VBA, FSEA/VBA between the two patient groups. Chi-square tests were utilized to compare gender distribution between the two groups of patients. Statistical significance was set at P < 0.05.

Results

Clinical characteristics of participants

A total of 50 patients with cervical SCI, meeting both the inclusion and exclusion criteria, were enrolled in the SCI group. This group included 26 males and 24 females, with an average age of (59.60 ± 10.81) years. Simultaneously, 50 age-matched individuals from the general population, undergoing routine physical examinations and meeting the inclusion criteria for the normal group, were recruited. The normal group consisted of 28 males and 22 females, with an average age of (55.00 ± 8.21) years. The general characteristics of the two groups are summarized in Table 2. There were no statistically significant differences between the groups in terms of gender, age, or C4-7 VBA.

Comparison of paravertebral extensor area and fat infiltration between the two groups

There were no statistically significant differences between the two groups in terms of the DEA and SEA at the C4-C7 levels. However, in the SCI group, both DFIR and SFIR at the C4-C7 levels were significantly higher compared to the normal group, with statistically significant differences (P < 0.001). Additionally, at the C5 and C6 levels, the FDEA/VBA and FSEA/VBA in the SCI group were lower than those in the normal group (FDEA/VBA _C5; P < 0.001, FDEA/VBA _C6; P < 0.001, FSEA/VBA _C5; P = 0.034; SEA/VBA _C6; P = 0.004). However, there were no statistically significant differences in FDEA/VBA and FSEA/VBA between the two groups at the C4 and C7 levels (Table 3).

Comparison of paravertebral extensor area and fatty infiltration in patients with mild and severe symptoms of cervical SCI

In patients with cervical SCI, symptom severity was categorized into mild and severe groups, and comparisons were made between paraspinal muscle and fat infiltration levels. The results indicated no statistically significant differences in DEA, SEA, DFIR, SFIR, FDEA/VBA, and FSEA/VBA between the two groups of patients (Table 4).

Comparison of paravertebral extensor area and fatty infiltration between genders in patients with cervical SCI

In SCI group, males exhibited significantly higher levels of DEA and SEA compared to females, with statistically significant differences (P < 0.001). However, there were no statistically significant differences between males and females in terms of DFIR and SFIR. At the C6 and C7 levels, the FDEA/VBA and FSEA/VBA in the male group were higher than those in the female group, with statistically significant differences (FDEA/VBA _C6; P = 0.009, FDEA/VBA _C7; P = 0.022, FSEA/VBA _C6; P = 0.019, FSEA/VBA _C7; P = 0.005). Conversely, at the C4 and C5 levels, there were no statistically significant differences between male and female patients (Table 5).

Table 2 Baseline patient characteristics

Table 3 Comparison of paravertebral extensor area and fatty infiltration between the two groups

Table 4 Comparison of paravertebral extensor area and fatty infiltration in patients with mild and severe symptoms of cervical SCI

Table 5 Comparison of paravertebral extensor area and fatty infiltration between genders in patients with cervical SCI

Discussion

This study reveals that patients in the cervical spinal cord injury group exhibit higher levels of fat infiltration compared to individuals without injuries, and the FDEA/VBA and FSEA/VBA at the C5 and C6 levels are lower in the control group. Patients with cervical spinal cord injury demonstrate diminished cervical spine stability and muscle protection relative to healthy individuals, rendering them more vulnerable to spinal cord involvement from external forces. The magnitude and mechanism of direct external forces are primary factors contributing to this susceptibility. Existing research consistently demonstrates the protective role of neck muscles in mitigating traumatic neck injuries [18]. Recent focus has shifted towards the role of cervical paraspinal muscles in maintaining spinal stability and function. The cervical paraspinal muscles are pivotal in supporting both static and dynamic functions of the cervical spine, crucial for postural stability, movement control, and load-bearing capacity [19, 20]. Changes in the composition and quality of these muscles have been linked to an increased risk of degenerative cervical spine conditions such as cervical spondylosis and intervertebral disc degeneration. Despite the expanding literature in this domain, few studies have directly compared cervical paraspinal muscle characteristics between patients with acute cervical SCI and healthy individuals. This study highlights significant degenerative changes observed in the cervical paraspinal muscles of acute cervical SCI patients compared to normal controls, emphasizing potential implications for spinal stability and functional outcomes. Further exploration of the mechanisms underlying these muscle alterations and their correlation with clinical outcomes is essential to guide targeted rehabilitation strategies and improve the management of cervical SCI.

Previous studies have indicated that patients with chronic spinal cord injuries often exhibit an increased fat infiltration ratio (FIR) in paravertebral muscles [21,22,23]. However, this study focuses on FIR during acute injury. Patients demonstrated higher FIR, extensor muscle degeneration, and decreased muscle mass compared to the normal population prior to injury. Liang et al. [24]. demonstrated that the C4-C6 region is a focal point of stress on the cervical spine. In this study, the FDEA/VBA and FSEA/VBA at the C5 and C6 levels were lower in the cervical spinal cord injury group compared to the control group, indicating weaker muscle protection and higher stress on the muscles at these levels during trauma. This finding aligns with epidemiological data showing high-risk zones for intervertebral disc injury in whiplash cases. Clinically, pathological conditions such as cervical disc protrusion and spinal canal stenosis are observed in some patients with cervical spinal cord injuries, potentially increasing their vulnerability to spinal cord damage. Further investigation is needed to explore the relationship between cervical paraspinal muscle degeneration and these pathological conditions.

Patients with cervical spinal cord injuries were classified into severity groups based on the ASIA classification, with no statistically significant differences observed between the groups. This could be attributed to the grouping method, suggesting the need for validation with larger sample sizes in future studies. Additionally, this study assessed gender differences in paravertebral extensor muscles and FIR among patients with cervical spinal cord injuries. While no significant differences in FIR were found between men and women, notable disparities were observed in DEA and SEA between the genders. Specifically, at the C6 and C7 levels, the FDEA/VBA and FSEA/VBA were higher in males compared to females, indicating greater development of paravertebral muscles in males, consistent with findings by Li et al. [11]. However, Egon et al. [25]. reported in their study on gender differences in FIR in the general population that male FIR was significantly lower than that of females. Therefore, the debate over gender differences in FIR among patients with acute cervical spinal cord injuries remains unresolved.

This study has several limitations. It is a single-center retrospective study with a relatively small sample size, highlighting the need for larger sample sizes and multicenter prospective studies to enhance reliability. Given that many patients with cervical spinal cord injuries also present with conditions like cervical disc herniation and spinal canal stenosis, further analysis to elucidate these correlations is warranted. The cervical spine, being the most intricate segment of the spine concerning movement, possesses a complex structure and composition of surrounding muscle groups. This study specifically focuses on the posterior paravertebral extensor muscles, which introduces certain constraints in its scope.

Conclusions

In summary, this study highlights that patients with acute cervical spinal cord injuries demonstrate elevated levels of fat infiltration and more extensive degeneration of paravertebral extensor muscles compared to the general population. Clinicians should closely monitor patients who exhibit concurrent fat infiltration in these muscles, especially those at risk of spinal cord injury. Proactive measures are essential to manage disease progression effectively. Strengthening exercises targeting neck muscles could be advised based on muscle and fat infiltration assessments, aiming to mitigate paravertebral extensor muscle degeneration and reduce the likelihood of cervical spinal cord injury.