Relationship between straight leg-raising test measurements and area of fat infiltration in multifidus muscles in patients with lumbar disc hernation

Abstract

BACKGROUND:

A few studies have noted that paraspinal muscle training is important to reduce pain for patients with lumbar disc herniation (LDH). However, little is known about the exact signs for necessary training of lumbar multifidus muscles (LMM).

OBJECTIVE:

The study aimed to analyze the relationship between the straight leg-raising test (SLR) and the area of fat infiltration in LMM for patients with LDH.

METHOD:

One hundred and fourteen LDH patients were involved in this study. Clinical data were collected from a medical record system. On the MRI images, the cross-sectional areas (CSA) of bilateral fat infiltration in LMM were measured by picture archiving and communication system (PACS).

RESULT:

For 61 patients with inclusive LDH, the positive side of SLR was positively correlated with the side of the larger total CSA of fat infiltration in LMM of L2-S1 ( $r=$ 0.75, $p ï ¼ œ$ 0.01), and the CSA of fat infiltration on the side of SLR with a positive result was significantly larger than that on the side of SLR with a negative result only at L3-4 and L4-5 levels ( $p ï ¼ œ$ 0.01).

CONCLUSION:

SLR may be used as an important sign for dysfunction of LMM and can identify the more severe side.

Keywords

Multifidus muscle disc herniation fat infiltration straight leg-raising test

Table 1
Descriptive statistics of the studied sample ( $n=$ 82 )

Variables	Total (%)	Male (%)	Female (%)	ES
Cases (n)	82	40 (48.8)	42 (51.2)	–
Age (years)	56.15 $\pm$ 18.42	51.85 $\pm$ 18.93	60.05 $\pm$ 17.86	0.2
Course (Months)	7.47 $\pm$ 13.31	9.48 $\pm$ 19.26	5.27 $\pm$ 7.02	0.1
Combined with LSS (n)	21 (25.6)	9 (42.9)	12 (57.1)	–
SLR(+) on the left (n)	42 (51.2)	20 (47.6)	22 (52.4)	–
SLR(+) on the right (n)	40 (48.8)	21 (52.5)	19 (47.5)	–
CSA of fat infiltration in LMM of L2-3 (mm ${}^{2}$ )	43.46 $\pm$ 24.83	32.42 $\pm$ 27.97	52.21 $\pm$ 21.65*	0.4
CSA of fat infiltration in LMM of L3-4 (mm ${}^{2}$ )	112.78 $\pm$ 55.09	85.31 $\pm$ 81.12	139.34 $\pm$ 56.34*	0.6
CSA of fat infiltration in LMM of L4-5 (mm ${}^{2}$ )	228.14 $\pm$ 101.13	233.36 $\pm$ 100.32	221.51 $\pm$ 102.68	0.3
CSA of fat infiltration in LMM of L5-S1 (mm ${}^{2}$ )‘	457.69 $\pm$ 147.20	423.43 $\pm$ 164.61	481.15 $\pm$ 156.43*	0.4

SLR: straight leg-raising test. (+): positive result. CSA: cross-sectional area. LSS: lumbar spinal stenosis. ES: effect size. Data were presented as mean $\pm$ SD. *Significantly different from male, $P<$ 0.01.

1. Introduction

Despite advances in spinal surgery including endoscopic surgery for lumbar disc herniation (LDH), recent studies on postoperative low back pain have reported high rates of persistent opioid use many years after lumbar surgery [1]. The pain caused by paraspinal muscles and nerves lesion lowers the quality of life in patients [2, 3]. After investigating the relationship between intramuscular pressure or blood flow during posterior lumbar surgery, a study found that paraspinal muscles degeneration after surgery could be explained by direct mechanical damage and increased intramuscular pressure of muscle tissue by the surgical instruments [4]. Several authors have also suggested that stability training involving paraspinal muscles can reduce pain and prevent recurrence after surgery [5, 6, 7, 8, 9, 10, 11]. Among paraspinal muscles, the function of lumbar multifidus muscles (LMM) is to maintain the normal physiological curvature of the lumbar and is considered to be the most important muscle for lumbar segmental stability [12, 13, 14]. In several imaging studies, low back pain has been proven to be related to fat infiltration of LMM [15, 16, 17, 18], while fat infiltration is an important feature of degenerating LMM that predominates in the lumbar spine [19, 20, 21, 22]. It is thought that atrophy of LMM is a result of immobilization and neural compression caused by a herniated disc [23, 24]. Straight leg-raising test (SLR) test is an important sign of spinal nerve root compression for patient with LDH [25, 26].

With the rapid development of evidence-based medicine, evidence should be incorporated into all aspects of clinical care, including rehabilitation of the spine [27]. Nevertheless, we found that only a few exercises are possible after lumbar surgery due to the pain [28, 29]. According to a study by Kim et al., many patients with LDH after lumbar surgery received manipulative rehabilitation (including LMM training), following a protocol only from experience [30]. Thus, studying precise indications for lumbar training is an important consideration and prerequisite to high-quality rehabilitation. To study this issue, Battié et al. [16] found a statistical correlation between the greater side of multifidus signal intensity (fat infiltration) and the side of the herniation at the level below the herniation. Furthermore, due to the direct intervertebral attachments, LMM is potentially better in providing intersegmental stability and its function is a frequent goal of rehabilitation of lumbar [31]. Consequently, clinicians began to investigate the markers of rehabilitation of LMM by imaging technology, such as ultrasound, CT and MRI [29, 31, 32]. However, imaging results and clinical signs are not exactly same. Therefore, the aim of this study was to analyze the relationship between SLR measurements and area of fat infiltration in LMM in patients with LDH and to determine if SLR could be used as an important sign for degenerating LMM to suggest the more severe side. Based on our understanding of the scientific literature in this area, we hypothesized that sciatica on one side caused by LDH leads to altered neuro-muscular functioning, which in turn results in atrophy of LMM on the same side, which is seen as fat infiltration. Moreover, no similar studies had mentioned the exact association between SLR and area of fat infiltration in LMM for patients with LDH before.

Figure 1.

Bilateral CSA of fat infiltration was obtained in lumbar multifidus at each level.

2. Materials and methods

2.1 Participants

This study retrospectively followed 114 patients with LDH who initially came to our clinic for percutaneous transforaminal endoscopic discectomy (PTED) between March 2017 and November 2017 in the Pain and Rehabilitation Medicine Centre of Navy General Hospital. Demographic details, duration of symptoms and clinical data including angular degree of SLR were recorded from patients’ medical records. In all, 32 cases were excluded for the following reasons: 10 had no records of SLR, 14 had no records of Magnetic Resonance Imaging (MRI), or only computed tomography or X-ray films, 3 had a history of severe spinal trauma, 2 had a space occupying the lesion of the spine, and 2 had diagnoses were not in accordance with the description of medical records. Inclusion criteria were as follows: (1) Patients met the diagnostic criteria of LDH according to the medical records and final diagnosis; (2) Posterolateral disc herniation at the following disc levels: L4-5 and L5-S1. Primary exclusion criteria were as follows: (1) Diseases of the spinal canal caused by metastatic tumor or spine infection; (2) History of spinal trauma or spinal deformity; (3) Syndrome of cauda equina; (4) Permanent disability of the lower limbs; (5) Incomplete medical records. Finally, 82 patients (42 females and 40 males) were included, of which 21 had combined lumbar spinal stenosis (LSS). The mean age of the subjects was 56.15 $\pm$ 18.42 years. The mean time from symptom onset to imaging was 7.47 $\pm$ 13.31 months. Positive sides of SLR were on the left in 42 subjects and on the right in 40 subjects (Table 1). This study was approved by the ethics committee of our hospital. All the included patients were informed about the study and all signed an informed consent form.

2.2 SLR test methods

With the patient lying down on his or her back on an examination couch, the examiner lifts the patient’s leg while the knee is straight. If the patient experiences sciatic pain when the straight leg is at an angle less than 70 degrees, then the test is positive. Otherwise it is negative.

Table 2
Comparison of CSA of fat infiltration in mm ${}^{2}$ for two sides with SLR(+) and SLR(-)

Level	CSA of fat infiltration on the side of SLR(+)	CSA of fat infiltration on the side of SLR(-)	t	$p$	ES
82 patients with LDH
L2-3	26.07 $\pm$ 28.85	19.00 $\pm$ 22.93	0.329	0.744	0.2
L3-4	60.27 $\pm$ 43.62	53.47 $\pm$ 45.71	0.417	0.680	0.2
L4-5	126.60 $\pm$ 65.49	137.27 $\pm$ 104.65	0.335	0.740	0.3
L5-S1	216.53 $\pm$ 115.31	224.47 $\pm$ 149.16	0.163	0.872	0.2
L2-S1	425.47 $\pm$ 177.61	433.80 $\pm$ 287.73	0.095	0.925	0.1
61 patients with inclusive LDH
L2-3	25.60 $\pm$ 21.01	18.53 $\pm$ 16.24	0.752	0.457	0.3
L3-4	51.49 $\pm$ 28.59	38.20 $\pm$ 21.86	2.477	0.015	0.5
L4-5	106.59 $\pm$ 49.89	73.19 $\pm$ 38.75	4.206	0.000	0.6
L5-S1	180.50 $\pm$ 106.19	170.99 $\pm$ 98.45	0.304	0.763	0.3
L2-S1	337.92 $\pm$ 149.04	285.39 $\pm$ 157.20	0.874	0.391	0.2

SLR: straight leg-raising test. (+): postive result. (-): negative result. CSA: cross-sectional area. LDH: lumbar disc herniation. ES: effect size. Data were presented as mean $\pm$ SD.

2.3 MRI methods

Three spinal doctors, who had been trained professionally and had been qualified, were responsible for collecting MRI data and for data processing. Lumbar MRI was performed used Siemens 3.0 T Magnetom vision and patients were placed in the prone position in the MRI device. The picture archiving and communication system (PACS) was applied to analyze the T2-weighted axial images at the inferior endplate of L2, L3, L4 and L5 bilaterally. On the endplate levels the contour line was constructed by polygon points around the outer edge of the fat infiltration in LMM. For details see Fig. 1. The measurements were performed separately for the right and left sides. To reduce the error of measuring, all the mean values were calculated from the three physicians mentioned above, including L2-S1 in total. Total CSA ${}_{L2-S1}$ $=$ CSA ${}_{L2-3}$ $+$ CSA ${}_{L3-4}$ $+$ CSA ${}_{L4-5}$ $+$ CSA ${}_{L5-S1}$ . The above mentioned methods were referred to in the study by Kjaer [33] and Li [34], and there is also evidence that this measure of fat infiltration in LMM, which uses MRI images, is reliable [35, 36].

2.4 Statistical evaluation

Statistical analyses of the findings were performed with the SPSS for Windows v.10.0 software program. Data were presented as mean $\pm$ SD. The differences between the CAS on the side of SLR with a positive result and the other side in LMM were compared by the Mann-Whitney U test since all data corresponded to the Gaussian distribution. Spearman’s correlation coefficient was applied to analyze the correlation between the side with a more severe degree of muscular degeneration degree (muscular fatty infiltration) and the positive side of SLR. Pearson’s correlation coefficient was applied to analyze the correlation between the area size of the degree of muscular degeneration and the angle size of SLR. Moreover, effect size (ES) has been defined as [37]: “the degree to which the phenomenon is present in the population” and the magnitude of ES has been interpreted as an index of clinical relevance [38, 39], so ES was be used as a indicator of clinical relevance in this study for SLR and CSA of fat infiltration in LMM.

$\overline{ES}=\frac{\overline{X_{G1}}-\overline{X_{G2}}}{S_{\textit{pooled}}}$

where: $ES=$ effect size, $X_{G1}=$ mean group 1, $X_{G2}=$ mean group 2, Spooled: pooled standard deviation (SD). An effect size of $ES\geqslant$ 0.4 was considered clinically relevant and more details about the counting process can be found in Armijo-Olivo et al. [39]. Statistical significance was accepted as $p<$ 0.05.

3. Results

In accordance with a prior study [33], we also found that the mean CSA of female was larger than that of males at L2-3, L3-4 and L5-S1 levels ( $p ï ¼ œ$ 0.01), while female participants had a markedly larger total CSA in LMM at L2-S1 ( $p ï ¼ œ$ 0.01) and these differences were considered clinically significant (all $ES\geqslant$ 0.4) (Table 1). The CSA in LMM of each segment was significantly larger than that of the last segment in L2-S1 (all $p ï ¼ œ$ 0.01) (Table 1).

Although not quite the same as the findings of Hides et al. [40], we found that the CSA of fat infiltration on the side of SLR(+) was significantly larger than that on the side of SLR(-) , but only at L3-4 and L4-5 levels for 61 patients with inclusive LDH ( $p ï ¼ œ$ 0.05 and $p ï ¼ œ$ 0.01). And the differences also were considered clinically significant (all $ES\geqslant$ 0.4) (Table 2). However, no significant asymmetry in CSA of fat infiltration was observed at other segments. In addition, side-to-side differences in CSA of fat infiltration did not reach statistical significance for patients with LDH (including 21 patients combined with LSS) (Table 2).

In contrast to our hypothesis, we found no correlation between the side of the larger CSA of fat infiltration and the side of straight leg raising with a positive result at any single level for 82 patients, including L2-3/L3-4/L4-5/L5-S1 (all $p ï ¼ ž$ 0.05) (Table 3). However, for 61 patients with inclusive LDH, there was a significant correlation between the side of SLR with a positive result and the side of the larger total CSA of fat infiltration at the L2-S1 level ( $r=$ 0.84, $p ï ¼ œ$ 0.01), where the mean total CSA was larger on the side of straight leg raising with a positive result in general (Table 3). No significant correlation of the side at any single level for patients with inclusive LDH was observed (all $p ï ¼ ž$ 0.05) (Table 3).

Table 3
Correlations between the sides of the larger CSA of fat infiltration in LMM and the sides of SLR with a positive result

Variables	The side of SLR (+)
	r	$p$
82 patients with LDH
(Including patients combined with LSS)
The side of the larger CSA of fat infiltration at L2-3 level	0.00	0.472
The side of the larger CSA of fat infiltration at L3-4 level	0.23	0.351
The side of the larger CSA of fat infiltration at L4-5 level	0.19	0.195
The side of the larger CSA of fat infiltration at L5-S1 level	0.42	0.152
The side of the larger tatal CSA of fat infiltration at L2-S1 level	0.21	0.205
61 patients with inclusive LDH
(Not including patients combined with LSS)
The side of the larger CSA of fat infiltration at L2-3 level	0.01	0.370
The side of the larger CSA of fat infiltration at L3-4 level	0.00	0.421
The side of the larger CSA of fat infiltration at L4-5 level	0.43	0.162
The side of the larger CSA of fat infiltration at L5-S1 level	0.38	0.258
The side of the larger tatal CSA of fat infiltration at L2-S1 level	0.74	0.001

SLR: straight leg-raising test. (+): positive result. CSA: cross-sectional area. LDH: lumbar disc herniation.

We also found that there were no significant correlations between the sizes of the larger CSA of fat infiltration and the angular degree of SLR with a positive result for patients with LDH (all $p ï ¼ ž$ 0.05) (Table 4).

Table 4

Correlations between the area sizes of the larger CSA of fat infiltration and the angular degree of SLR with a positive result

Variables	The angular degree of SLR(+)
	r	$p$
82 patients with LDH
(Including patients combined with LSS)
The larger CSA of fat infiltration at L2-3 level	0.02	0.394
The larger CSA of fat infiltration at L3-4 level	0.45	0.106
The larger CSA of fat infiltration at L4-5 level	0.00	0.425
The larger CSA of fat infiltration at L5-S1 level	0.08	0.404
The larger tatal CSA of fat infiltration at L2-S1 level	0.31	0.227
61 patients with inclusive LDH
(Not including patients combined with LSS)
The larger CSA of fat infiltration at L2-3 level	0.00	0.514
The larger CSA of fat infiltration at L3-4 level	0.20	0.116
The larger CSA of fat infiltration at L4-5 level	0.23	0.130
The larger CSA of fat infiltration at L5-S1 level	0.08	0.380
The larger tatal CSA of fat infiltration at L2-S1 level	0.15	0.172

LR: straight leg-raising test. (+): positive result. CSA: cross-sectional area. LDH: lumbar disc herniation.

4. Discussion

Our study included lumbar levels from L2-3 to L5-S1, and not only L4-5 and L5-S1 as Battié’s study [16] included, mainly considering that LMM is a group of muscles which stretches across several lumbar vertebral segments. In addition, given that statistical significance does not offer an indication of how important the result of the study is [41], ES was included in our study. As is apparent from Table 1, the CSA in LMM of each segment was significantly larger than that of the last segment in L2-S1, and the sexual differences of CSA were considered clinically significant in L2-3 and L3-4 (all $ES\geqslant$ 0.4). Therefore it is not very reliable to analyze just one or two segments. Meanwhile, it is supposed that clinical signs of the patient are reliable hints for functional change, and not just for the imaging results due to sexual differences. For example, large central protrusion may cause symptoms of the left or right lower extremity. Thus, we chose a clinical sign (SLR) as a research goal and analyzed the relationship between SLR and LMM.

The difference between the side of SLR(+) and SLR(-) was found in present study, and it indicated that the CSA of fat infiltration in LMM on the side of SLR(+) is larger than the other side at L4-5 levels for 61 patients with inclusive LDH (Table 2). Note that this difference was considered both statistically significant and clinically significant. However, for L3-4, although $P$ value did not reach 0.01, ES indicated that a clinically important difference between the side of SLR(+) and SLR(-). Based on the above, although variability of the CSA of fat infiltration in LMM was high at L3-4, subjects with SLR(+) were considered to have a strong tendency to have more severe fat infiltrations compared with SLR(-). For 82 patients, some of which had combined LSS, this difference had not been observed. Likewise, for patients with inclusive LDH, there was a significant correlation between the side of SLR(+) and the side of the larger tatal CSA of fat infiltration at L2-S1 level, although we know that SLR(+) suggests the compression of the sciatic nerve which come from L4 and lower nerve roots. And once including 21 patients combined with LSS, this correlation also had not been observed at any single level (Table 3). In addition, it is remarkable that few studies about the study of LMM in LSS patients can be found. One possible reason may be that LMM is affected not only by nerve lesions but also by many degenerative changes for LSS, including thickening of ligamentum flavum, lumbar scoliosis, lumbar lordosis, lumbar osteoporosis and other influencing factors from LSS. However, for inclusive LDH, there is only one pathogenic factor (disc herniation). These results are in accordance with the pathological results from Millis [41], who found that patients with a long duration of radicular symptoms originating from lumbar disc herniation have an increased risk for pathologic muscular changes.

For inclusive LDH in our study, it is obvious from Tables 2 and 3 that we may determine the side of dysfunctional LMM by the side of SLR with a positive result, which can be confirmed further by the CSA of fat infiltration at L3-4 and L4-5 levels. However, according to Table 4, the degree of degeneration of LMM cannot be evaluated by the degree of SLR, since there were no significant correlations between the sizes of the larger CSA of fat infiltration in LMM and the angular degree of SLR with a positive result for patients with LDH.

There were several limitations in this study. The first problem is the measure of fat infiltration in LMM. There were many tiny and scattered fat gaps in LMM, and so we could not construct the contour line accurately around the outer edge of the tiny fat infiltration on MRI. Thus, the measure of CSA of partial fat infiltration was not very precise. In addition, it was difficult to exclude subjective factors completely although we had calculated a mean value of MRI data from three different professional physicians. Moreover, the approach may need to be different for males and females in future studies because there are gender differences on the CSA of LMM, according to Hides et al. [40]. Similarly, the present study also showed the significant difference between males and females (Table 1). The third problem is the low number of enrolled patients. If a larger number of subjects were included, the results may be more reliable.

In conclusion, the study findings suggest that SLR may be used as an important sign for dysfunction of LMM and can suggest the more severe side for inclusive LDH. However, the degree of degeneration of LMM can not be evaluated by the degree of SLR. We hope that this study may remind lumbar surgeons to protect the LMM during the operation.

Footnotes

Acknowledgments

This study was supported by the innovation fund of the Naval General Hospital (CXPY201721).

Conflict of interest

None to report.

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