Evaluation of the degeneration of the multifidus and erector spinae muscles in patients with low back pain and healthy individuals

Abstract

BACKGROUND:

Although several studies have been conducted to determine the cause of low back pain (LBP), a sufficient correlation has not been found between research findings and symptoms. Therefore there seems to be a need for studies to explain the relationship between pain and morphological changes in the paraspinal muscles of patients with LBP through comparisons with healthy control subjects.

OBJECTIVE:

The aim of this study was to examine degeneration in the lumbar musculus multifidus (LMF) and lumbar musculus erector spinae (LES) muscles in patients with chronic LBP with non-radiculopathy lumbar disc herniation (LDH), patients with mechanical LBP, and healthy individuals.

METHODS:

The study included 35 patients with mechanical LBP, 38 patients with non-radiculopathy LDH, and a control group of 36 healthy participants. In all patients and the control group, evaluations were made on axial magnetic resonance imaging slices at L3-S1 level of the LMF and LES cross-sectional areas (CSA), total CSA (TCSA $=$ LMF $+$ LES), fat infiltrations and asymmetries.

RESULTS:

The mean CSA values of the right and left LMF and LES showed significant differences between the groups ( $p<$ 0.001, $p=$ 0.002, $p=$ 0.002, $p=$ 0.010, respectively). Fat infiltrations showed a difference between the right-left LMF and left LES groups ( $p=$ 0.007, $p<$ 0.001, $p=$ 0.026, respectively). Asymmetry was not observed between the CSA and TCSA of the right and left sides.

CONCLUSION:

A correlation was found between fat infiltration in the LMF and mechanical LBP and LDH. However, no significant correlation was determined between LBP and the CSA and TCSA of the LMF and LES. This was thought to be due to an incorrect result of CSA and TCSA in the evaluation of muscle mass. Therefore, for a more accurate evaluation of muscle mass, it can be considered necessary to measure muscle atrophy associated with fat infiltration or functional CSA.

Keywords

Low back pain paraspinal muscles intervertebral disc displacement magnetic resonance imaging

1. Introduction

Low back pain (LBP) is a problem widely seen in the general population and is a social, psychological, and economic burden [1, 2, 3]. This renders it a socioeconomic health problem due to long-term morbidity, with loss of workforce causing high costs [4]. Several studies have been conducted to determine the causes of LBP and several mechanisms have been stated [5, 6, 7], but this area is lacking in clinical interpretations and examination methods.

Studies have shown that a circular tear of the disc and nerve growth factor in the region of degenerated discs increase inflammatory mediators and nociceptive factors and increase the sensitivity of nerve fibres in the disc, and all of these are likely sources of chronic LBP [5, 6]. In degenerated intervertebral discs, innervation has been shown to be intensely increased, including in regions where there has been no innervation, and this increasing innervation has been associated with pain of intervertebral origin [7].

The causes of LBP include lifestyle, working conditions, traumatic events, demographic characteristics, congenital malformations, and infectious, inflammatory, metabolic, neurogenic, neoplastic, and several other factors [1].

The paraspinal muscles play a secondary role in the structural and functional stabilisation of the lumbar spine. The paraspinal muscles are formed of the superficial muscle layer responsible for spine and extremity movements, which primarily control intersegmentary movement, and the deep muscle layer (LMF and LES), which function in lumbar stabilisation [8, 9, 10, 11, 12]. The primary function of the paraspinal muscles is to provide extension of the spine. In addition, when the LES moves unilaterally, it assists lateral flexion. Compared to all other lumbar muscles, the LMF is short, thick, and has a large cross-sectional area (CSA). These properties allow the LMF to produce very large forces in a short time and make the LMF ideal for stability [13, 14, 15, 16]. In contrast to the multisegmental innervation of the paraspinal muscle system, the LMF has unilateral innervation originating from the medial branch of the posterior root of the segmental nerve [17].

Fat infiltration (fat tissue entering muscle tissue), fibrosis (collagen connective tissue replacing normal muscle tissue) and atrophy (reduced contractile protein volume, that is, reduced cross-sectional area of the muscle and muscle cells) have been stated as the characteristics of muscle degeneration [18, 19, 20, 21, 22]. In the process of muscle degeneration, a decrease in muscle dimensions, an increase in adipose tissue activation, and early fat infiltration are seen in the acute period, and in the subacute period, type I slow muscle fibres transform to type II rapid muscle fibres (type I fibres are responsible for muscle strength and endurance), changes occur at the cellular and molecular level, fibrosis develops, and there is an increase in fat infiltration. The chronic period refers to the continued increase in atrophy of the muscle and muscle fibres, fibrosis and fat infiltration [15, 16, 23, 24, 25, 26, 27]. In a study by Pakkola et al, there was shown to be 9% fat infiltration in the paraspinal muscles of healthy middle-aged volunteers [19].

Several studies have been conducted to determine the condition of the paraspinal muscles in patients with LBP, and these studies have produced different results. The duration of pain [8, 28, 29, 30], and the size of the paraspinal muscles have been associated with gender [31, 32, 33, 34], Body Mass Index (BMI) [28, 33, 35, 36], level of physical activity, the efficacy of exercises [37, 38] and familial history [35]. The combined effects of familial genes and the shared early environment have been reported to be the strongest indicator of paraspinal muscle parameters [28]. In patients with LDH, paraspinal muscle atrophy is thought to be due to non-use, denervation and re-innervation. The muscle denervation forming in disc herniations has been stated to lead to rapid atrophy together with the sheath of the contractile mass in the skeletal muscle or progressive degeneration of the muscle fibrils, increased fatty tissue within the muscle and changes in muscle fibre type, irregular cell populations, altered gene expression, low muscle resistance, and low muscle strength [5, 27, 30]. Experimental studies have reported that in chronic LBP patients there are more type I rapid glycolytic fibres than type I slow oxidative fibres in the LMF and LES [23, 39, 40, 41, 42], that this type of fibre structure emerges with symptom duration [23] and this type of fibre structure leads to fatigue and less resistant paraspinal muscles [43].

Magnetic resonance imaging (MRI) is a non-invasive method for the evaluation of the paraspinal muscle tissue structure and components, which has come into widespread use in recent years for the detection of changes associated with diseases, response to injuries, or mechanical stress [44, 45]. MRI provides a clear image with high resolution and contrast for soft tissue, without radiation exposure, giving information about muscle CSA and fat infiltration. It has also been stated that the reliability of MRI is slightly better than that of computed tomography (CT) [46].

The aim of this study was to examine the morphology of the multifidus and erector spinae muscles in patients with chronic low back pain of mechanical and lumbar herniated disc origin, and a healthy control group and to determine whether or not different treatment approaches are required for these patient groups, especally for the treatment of LBP. A secondary aim was to evaluate the relationships in all three groups between the size and fat infiltration of the paraspinal muscles and the age, gender, BMI, and level of segmental involvement (L3-L4, L4-L5, L5-S1). A third aim was to evaluate the relationship between the size of the paraspinal muscles, fat infiltration, and the duration and severity of pain in the mechanical LBP and lumbar disc herniated groups.

Figure 1.

Flowchart of the selection of participants for the study.

2. Method

2.1 Participants

This observational, cross-sectional study was conducted between November 2020 and February 2021 with 109 participants. A control group was formed of 36 healthy individuals, selected at random from volunteers who responded to the invitation through social media and announcements, and who were not determined with any low back problem in physical examination and radiological screening and described no LBP within the last year. The mechanical LBP group (non-specific LBP) was formed of 35 patients who presented at the Orthopaedics and Traumatology Department with the complaint of LBP, had no additional lower back problem, and were not determined with any additional lumbar problem in physical examination, radiological screening (on MRI), or laboratory tests, and had not received any low back pain treatment. The lumbar disc herniation (LDH) group included 38 patients determined with lumbar disc herniation only on MRI, with no findings of root compression on examination and no complaints of radicular pain, and had not received any low back pain treatment. EMG was requested for patients when there was suspicion of root compression. Patients determined with root compression on MRI and EMG, and those with degenerative disc disorders were not included in the herniated lumbar disc group. The participants in all three groups were aged 20–65 years. The patients in the mechanical LBP group and in the LDH group were selected at random from patients with LBP ongoing for 3 months (Fig. 1). Both groups were similar in respect of the pain duration (chronic pain) and character (widespread pain for which localisation in the low back could not be clearly stated). Differentiation was made with the determination of lumbar disc herniation on MRI.

LBP was defined as pain between the lower border of the costae and the gluteal fold. The demographic, clinical, and disease-related data of all participants were obtained in face-to-face interviews. Hemogram, erythrocyte sedimentation rate, full urine analysis, salmonella, brucella, anti-streptolysin O (ASO), rheumatoid factor (RF), and C-reactive protein (CRP) tests were applied to patients when a differential diagnosis was necessary. Pain severity was evaluated with the Visual Analog Scale (VAS).

As seen in the flow chart (Fig. 1), 66 participants who did not describe LBP within the last year were initially enrolled for the healthy control group. After the exclusion of 23 who did not meet the study inclusion criteria, and 7 who were determined with disc hernation radiologically, a total of 36 healthy participants were included in the study. For the mechanical LBP group, 64 patients who presented at the Orthopaedics polyclinic were initally enrolled. After the exclusion of 12 patients who did not meet the study inclusion criteria, 1 who did not wish to participate in the study, and 16 determined radiologically with disc herniation, 35 patients were included in this group for the study. For the LDH group, 66 patients who presented at the Orthopaedics polyclinic were initally enrolled. After the exclusion of 14 patients who did not meet the study inclusion criteria, 3 who did not wish to participate in the study, and 6 determined with radiculopathy in the radiological screening and 5 determined with spondylolisthesis and spondyloarhtrosis, a total of 38 patients were included in this group for the study.

Study inclusion criteria

•
Age range of 20–65 years for the healthy control group, mechanical LBP group and the LDH group,
•
LBP ongoing for the last 3 months for the mechanical LBP and LDH groups,
•
Only lumbar disc herniation determined on MRI for the LDH group.

Study exclusion criteria

•
For the healthy control group, the presence of LBP or lumbar problem determined on radiological screening,
•
For the mechanical LBP group, lumbar disc herniation determined on radiological screening,
•
For the LDH group, the presence of radicular pain, or the determination of findings of root compression on EMG, radiological screening, or in the physical examination,
•
For all three groups, regular physical activity, the presence of additional inflammatory (ankylosing spondylitis), infectious, metabolic, neoplastic, or hip and pelvis disorder, limb shortness, neurogenic disorder, vertebral fracture, structural deformity malformations (scoliosis, kyphosis), genitourinary system problems, or a history of lumbar surgery.
•
Patients receiving lumbar treatment.

The examinations of 109 participants were made by the same experienced spine surgeon and the lumbar spine MR images were analyzed by the same experienced radiology specialist, who was blinded to the clinical history. All MRIs were taken by the same radiology technician. In the physical examination for differential diagnosis, specific lumbar segmental instability orthopaedic tests were applied (paravertebral intervertebral movement test, prone instability test) and the specific tests applied to determine radiculopathy (straight leg raise test, contralateral straight leg raise, laseque test, femoral nerve tension test) in herniated lumbar disc were negative. There was no loss of strength or sensory loss associated with nerve root compression in any of the patients. In the radiological examinations, no findings were determined on direct radiographs suggestive of fracture, deformity, infection, or neoplasm. On MRI, hernia types were classified as protrusion, extrusion, and extrusion subtype sequestration, based on the degree of median, paramedian, foraminal, and extraforaminal protrusion according to the localisation of the protruding section of the disc [47, 48]. As there was no radiculopathy in any of the patients, there was no need for an MRI-based nerve compression grading system.

Figure 2.
T2 sagittal and axial MR images of a healthy control group subject.

Approval for the study was granted by the Ethics Committee of the Scientific Research Board of Near East University (YDU/2020/83-1160). Written informed consent was obtained from all study participants before inclusion.
2.2 Measurements

2.2.1 Magnetic resonance imaging

Imaging was performed with a 1.5 Tesla MR device (Signa Explorer SV25.3 16 channel, up-to-date software, General Electric, Milwaukee, WI, USA). Following adjustment for the localisation, shots were taken with the patient positioned supine, with a routine protocol for the lumbar spine with the measurement level between L3-S1 at the center of the disc (Fig. 2). Turbo spin-echo T1 and T2-weighted sagittal and turbo spin-echo T2 axial 4 mm sections parallel to the disc spaces were taken. The fat content and CSA of the lumbar musculus multifidus and erector spinae were measured bilaterally at L3-S1 levels, with each level examined separately for comparisons of the CSA and TCSA and of left and right asymmetry. This range was included as diseases of the lumbar region are usually seen in the lower lumbar region (L3-S1) and the upper lumbar spine region was not included. In a study by Kalichmann et al. on CSA and fat infiltration of the paraspinal muscles, inter-observer reliability was reported to be moderate and the intra-observer agreement was excellent for the measurements on MRI [49].

There is no consensus about the T1 and T2-weighted sequences used in MRI. In most studies, degeneration has been classified using axial images. It has been stated that muscle, fat, and fascial structures are more easily determined and differentiated on T2-weighted slices (Fig. 2) [50]. Therefore, if the evaluation is semiquantitative, errors will be reduced to a minimum.

In the current study, the fascial borders (epimysium) of the CSA muscles were determined and measured using PACS report (picture archiving and communication system) imaging and manual drawing. Fat infiltration of the muscles was evaluated semiquantitatively as 1st degree: normal ( $<$ 10% fat infiltration of the CSA), 2nd degree: moderate (10%–50% fat infiltration), and 3rd degree: severe ( $>$ 50% fat infiltration) (Fig. 3) [2, 17, 20, 47]. Asymmetry was defined according to the larger side at L3-L4, L4-L5, and L5-S1 results. Asymmetry was calculated as “the largest edge – the smallest edge/the largest edge $\times$ 100” and stated as a percentage (%) [51].

Figure 3.

Fat infiltration degrees and localisation of the muscles on lumbar T2 axial MRI, Musculus multifidus (MF), Musculus erector spinae (ES), Musculus longissimus (LI), Musculus iliocostalis (IC) and, (ï¼¡) Grade 1: $<$ %10 fat infiltration; (B) Grade 2: 10%–50% fat infiltration; (C) Grade 3: $>$ 50% fat infiltration.

For internal reliability, 13 randomly selected patients were re-evaluated by the same radiologist after an interval of one month. The intra-observer kappa agreement value obtained was 0.941.

2.2.2 Statistical evaluation

Data obtained in the study were analyzed statistically using SPSS vn. 23 software (IBM Corp., Chicago, IL, USA). Taking the CSA mean values into consideration, it was determined to be necessary to have a minimum sample size of 78 participants for 95% confidence (1- $\alpha$ ), 95% test power (1- $\beta$ ) and effect size of $f=$ 0.461. To allow for sample loss, the study was completed with a total of 109 participants. According to the post hoc power analysis, the test power with 109 participants was determined as 99.3% [52].

Conformity of the data to normal distribution was assessed with the Kolmogorov-Smirnov test. In the comparisons of data not showing normal distribution, the Kruskal Wallis and Mann-Whitney U tests were applied. The main effects of group, gender, and segment on CSA and TCSA were examined with the MANCOVA test taking age and BMI as covariate variables. The Bonferroni test was used in multiple comparisons. In the examinations of categorical data according to groups, the Chi-square test was used. A value of $p<$ 0.05 was accepted as statistically significant. With MANCOVA analysis, segment was added to the model as an independent factor. Bonferroni correction was used to compare the main effects that were found to be significant in the model. The SPSS program automatically calculates the 95% confidence interval by making Bonferroni correction, and for this, Type 1 error is guaranteed.

3. Results

The demographic characteristics of the patients according to groups are shown in Table 1. No significant difference was determined between the groups in respect of age, gender, BMI, and duration of LBP ( $p=$ 0.631, $p=$ 0.808, $p=$ 0.815, $p=$ 0.737, respectively).

3.1 Examinations of the CSA and TCSA of the groups

The mean CSA values (Tables 2 and 3) in the right-left LMF and LES showed a difference between the groups ( $p<$ 0.001, $p=$ 0.002, $p=$ 0.002, $p=$ 0.010, respectively). The mean CSA value of the right LMF was determined to be lower in the healthy control group than in the mechanical LBP group and the herniated disc group, and there was no difference between the mechanical LBP group and the herniated disc group. The mean CSA values of the left LMF and right LES was determined to be lower in the healthy control group than in the herniated disc group, and the value in the mechanical LBP group was not found to be different from the others. The mean value in the left LES was determined to be similar in the healthy control group and the mechanical LBP group, and this was lower than in the herniated disc group. The mean right-left TCSA values were determined to be significantly different between the groups. This difference was due to the mean value of the healthy control group being lower than that of the herniated disc group ( $p<$ 0.001).

The mean CSA and TCSA values in all muscle groups were significantly different in the groups according to gender ( $p<$ 0.001) (Tables 2 and 3). The CSA and TCSA values of males were found to be higher than those of females in all 3 groups.

The CSA values were statistically significantly different in all groups according to the segments (L3-L4, L4-L5, L5-S1) ( $p<$ 0.001) (Tables 2 and 3). In all groups, the largest LMF CSA was determined at L5-S1 and the smallest at L3-L4, and the largest LES CSA was in the L3-L4 segment and the smallest in the L5-S1.

In the comparisons of asymmetry, the CSA and TCSA showed no difference between all groups ( $p>$ 0.05). No significant difference was determined in the mean right and left mean TCSA values according to segments ( $p>$ 0.05) (Table 2).

Table 1
Comparisons of the age, gender, BMI, duration of pain and pain severity (VAS score) of the patients according to the groups

Age (years)	36.36 $\pm$ 12.12	34 (26–44.5)	36.97 $\pm$ 13.6	32 (26–46)	37.92 $\pm$ 10.57	43.5 (27–46)	37.10 $\pm$ 12.02	38 (26–45.5)	0.631 ${}^{1}$
	Healthy ( $n=$ 36)		Mechanical ( $n=$ 35)		Herniated disc ( $n=$ 38)		Total ( $n=$ 109)		$P$ değeri
	$\bar{x}\pm\sigma$	Median (Q1-Q3)	$\bar{x}\pm\sigma$	Median (Q1-Q3)	$\bar{x}\pm\sigma$	Median (Q1-Q3)	$\bar{x}\pm\sigma$	Median (Q1-Q3)
BMI (kg/m ${}^{2}$ )	25.71 $\pm$ 3.63	25.93 (22.69–28.87)	25.84 $\pm$ 5.61	24.69 (20.57–32)	26.49 $\pm$ 5.14	26.4 (21.58–31.36)	26.03 $\pm$ 4.83	25.71 (21.64–30.09)	0.815 ${}^{1}$
LBP duration (months)			40.97 $\pm$ 59.74	8 (3–60)	38.95 $\pm$ 51.92	7 (3–63)	39.92 $\pm$ 55.42	7 (3–60)	0.737 ${}^{2}$
VAS rest			1.66 $\pm$ 0.8	1 (1–2)	2.39 $\pm$ 1.37	2 (1–3.25)	2.04 $\pm$ 1.18	2 (1–3)	0.022 ${}^{2}$
VAS activity			3.14 $\pm$ 0.94	3 (3–4)	4.37 $\pm$ 1.87	4 (3–6)	3.78 $\pm$ 1.61	3 (3–5)	0.006 ${}^{2}$
Gender	n (%)		n (%)		n (%)
Male	15 (41.7)		12(34.3)		14 (36.8)		41(37.6)		0.808 ${}^{3}$
Female	21 (58.3)		23(65.7)		24 (63.2)		68(62.4)

${}^{1}$ Kruskal Wallis, ${}^{2}$ Mann-Whitney U, ${}^{3}$ Pearson Chi Square, VAS: Visual Analog Scale, LBP: low back pain.

Table 2

Comparison of the groups according to CSA and TCSA, gender, segment, age, and BMI

		Group		Gender		Segment		Age		BMI
		$p$	$\eta^{2}$	$p$	$\eta^{2}$	$p$	$\eta^{2}$	$p$	$\eta^{2}$	$p$	$\eta^{2}$
CSA	Right LMF	$<$ 0.001	0.062	$<$ 0.001	0.148	$<$ 0.001	0.536	0.291	0.003	0.021	0.017
	Left LMF	0.002	0.039	$<$ 0.001	0.190	$<$ 0.001	0.554	0.972	$<$ 0.001	0.001	0.037
	Right LES	0.002	0.039	$<$ 0.001	0.174	$<$ 0.001	0.163	0.028	0.015	$<$ 0.001	0.126
	Left LES	0.010	0.029	$<$ 0.001	0.124	$<$ 0.001	0.145	0.001	0.037	$<$ 0.001	0.139
TCSA	Right LMF $+$ LES	$<$ 0.001	0.067	$<$ 0.001	0.236	0.085	0.015	0.145	0.007	$<$ 0.001	0.123
	Left LMF $+$ LES	$<$ 0.001	0.048	$<$ 0.001	0.219	0.057	0.018	0.002	0.031	$<$ 0.001	0.164

$\eta^{2}$ : partial eta squared, CSA: Cross-sectional area, TCSA: Total cross-sectional area, LMF: lumbar musculus multifidus, LES: lumbar erector spinae, BMI: Body Mass Index.

Table 3

The relationship between the segments, gender and CSA and TCSA measurements of the groups

	Right LMF (CSA)		Left LMF (CSA)		Right LES (CSA)		Left LES (CSA)		Right TCSA		Left TCSA
Groups
Healthy	936.92	$\pm$ 262.59 ${}^{\text{a}}$	945.09	$\pm$ 261.6 ${}^{\text{a}}$	1640.85	$\pm$ 450.58 ${}^{\text{a}}$	1679.92	$\pm$ 469.33 ${}^{\text{a}}$	2577.77	$\pm$ 455.4 ${}^{\text{a}}$	2625.01	$\pm$ 493.37 ${}^{\text{a}}$
Mechanical	1014.42	$\pm$ 352.06 ${}^{\text{b}}$	989.63	$\pm$ 331.65 ${}^{\text{ab}}$	1686.01	$\pm$ 651.16 ${}^{\text{ab}}$	1668.63	$\pm$ 615.93 ${}^{\text{a}}$	2700.43	$\pm$ 799.12 ${}^{\text{ab}}$	2658.26	$\pm$ 716.84 ${}^{\text{a}}$
Herniated disc	1054.67	$\pm$ 295.52 ${}^{\text{b}}$	1032.46	$\pm$ 282.93 ${}^{\text{b}}$	1849.68	$\pm$ 489.49 ${}^{\text{b}}$	1849.46	$\pm$ 525.05 ${}^{\text{b}}$	2904.34	$\pm$ 563.32 ${}^{\text{b}}$	2881.92	$\pm$ 574.16 ${}^{\text{b}}$
Gender
Male	831.78	$\pm$ 214.83	839.29	$\pm$ 197.61	2335.76	$\pm$ 533.98	2281.17	$\pm$ 522.29	3167.54	$\pm$ 666.39	3120.46	$\pm$ 617.87
Female	665.76	$\pm$ 135.36	663.62	$\pm$ 140.56	1688.35	$\pm$ 319.48	1705.65	$\pm$ 369	2354.12	$\pm$ 379.55	2369.26	$\pm$ 410.97
Segment
L3–L4	728.21	$\pm$ 187.05 ${}^{\text{a}}$	1041.7	$\pm$ 225.95 ${}^{\text{a}}$	1238.65	$\pm$ 257.98 ${}^{\text{a}}$	728.21	$\pm$ 187.05 ${}^{\text{a}}$	1041.7	$\pm$ 225.95	1238.65	$\pm$ 257.98
L4–L5	729.7	$\pm$ 184.47 ${}^{\text{b}}$	1016.83	$\pm$ 206.3 ${}^{\text{b}}$	1223.02	$\pm$ 246.76 ${}^{\text{b}}$	729.7	$\pm$ 184.47 ${}^{\text{a}}$	1016.83	$\pm$ 206.3	1223.02	$\pm$ 246.76
L5–S1	1931.87	$\pm$ 517.87 ${}^{c}$	1768.09	$\pm$ 386.43 ${}^{c}$	1484.5	$\pm$ 603.45 ${}^{c}$	1931.87	$\pm$ 517.87 ${}^{\text{b}}$	1768.09	$\pm$ 386.43	1484.5	$\pm$ 603.45

${}^{\text{a-b-c}}$ : No difference between groups/segments with the same letter, ${}^{\text{a-b-c}}$ : There is a difference between groups/segments with different letters, ${}^{\text{ab}}$ : The mean value does not differ from the other 2 groups, CSA: Cross-sectional area, TCSA: Total cross-sectional area, LMF: lumbar musculus multifidus, LES: lumbar erector spinae.

Table 4

Correlations between the groups of age, BMI, low back pain duration, and VAS scores

Group	Parameters	Age		BMI		LBP duration		VAS rest		VAS activity
Mechanical group
CSA	Right LMF (mm ${}^{2}$ )	0	.178	0	.209*	0	.068	$-$ 0	.570**	$-$ 0	.485**
	Left LMF (mm ${}^{2}$ )	0	.170	0	.243*	0	.101	$-$ 0	.413*	$-$ 0	.346*
	Right LES (mm ${}^{2}$ )	0	.423**	0	.506**	0	.204	$-$ 0	.294	$-$ 0	.275
	Left LES (mm ${}^{2}$ )	0	.359**	0	.549**	0	.216	$-$ 0	.380*	$-$ 0	.323
TCSA	Right LMF $+$ LES (mm ${}^{2}$ )	0	.403**	0	.537**	0	.153	$-$ 0	.431**	$-$ 0	.368*
	Left LMF $+$ LES (mm ${}^{2}$ )	0	.394**	0	.570**	0	.207	$-$ 0	.448**	$-$ 0	.365*
Herniated Disc group
CSA	Right LMF (mm ${}^{2}$ )	$-$ 0	.064	0	.031	$-$ 0	.012	$-$ 0	.142	$-$ 0	.002
	Left LMF (mm ${}^{2}$ )	$-$ 0	.057	0	.042	$-$ 0	.083	$-$ 0	.252	$-$ 0	.038
	Right LES (mm ${}^{2}$ )	$-$ 0	.037	0	.249**	$-$ 0	.098	$-$ 0	.210	$-$ 0	.071
	Left LES (mm ${}^{2}$ )	$-$ 0	.031	0	.175	$-$ 0	.193	$-$ 0	.112	0	.063
TCSA	Right LMF $+$ LES (mm ${}^{2}$ )	$-$ 0	.110	0	.176	$-$ 0	.118	$-$ 0	.236	$-$ 0	.086
	Left LMF $+$ LES (mm ${}^{2}$ )	$-$ 0	.071	0	.185*	$-$ 0	.198	$-$ 0	.128	0	.091
Healthy group
CSA	Right LMF (mm ${}^{2}$ )	0	.086	0	.166	$-$		$-$		$-$
	Left LMF (mm ${}^{2}$ )	0	.040	0	.206 ${}^{\ast}$	$-$		$-$		$-$
	Right LES (mm ${}^{2}$ )	$-$ 0	.172	0	.068	$-$		$-$		$-$
	Left LES (mm ${}^{2}$ )	$-$ 0	.228 ${}^{\ast}$	0	.154	$-$		$-$		$-$
TCSA	Right LMF $+$ LES (mm ${}^{2}$ )	$-$ 0	.121	0	.63	$-$		$-$		$-$
	Left LMF $+$ LES (mm ${}^{2}$ )	$-$ 0	.196 ${}^{\ast}$	0	.255 ${}^{\ast\ast}$	$-$		$-$		$-$
${}^{}<$ 0,05, ${}^{*}<$ 0.001 CSA: Cross-sectional area, TCSA: Total cross-sectional area, LMF: lumbar musculus multifidus, LES: lumbar erector spinae, BMI: Body Mass Index, LBP: Low back pain, VAS: Visual Analog Scale.

Table 5

Comparison of fat infiltrations between groups (Simplified 3-degree system)

N (%)	Healthy group		Mechanical group		Herniated Disc group		Total		$P^{*}$
Fat infiltration right LMF
$<$ 10%	46	(42.6) ${}^{\text{a}}$	21	(20) ${}^{\text{b}}$	38	(33.3) ${}^{\text{ab}}$	105	(32.1)	0.007
10%–50%	62	(57.4) ${}^{\text{a}}$	82	(78.1) ${}^{\text{b}}$	75	(65.8) ${}^{\text{ab}}$	219	(67)
$>$ 50%	0	(0) ${}^{\text{a}}$	2	(1.9) ${}^{\text{a}}$	1	(0.9) ${}^{\text{a}}$	3	(0.9)
Fat infiltration left LMF
$<$ 10%	49	(45.4) ${}^{\text{a}}$	19	(18.1) ${}^{\text{b}}$	42	(36.8) ${}^{\text{a}}$	110	(33.6)	$<$ 0.001
10%–50%	59	(54.6) ${}^{\text{a}}$	83	(79) ${}^{\text{b}}$	71	(62.3) ${}^{\text{a}}$	213	(65.1)
$>$ 50%	0	(0) ${}^{\text{a}}$	3	(2.9) ${}^{\text{a}}$	1	(0.9) ${}^{\text{a}}$	4	(1.2)
Fat infiltration right LES
$<$ 10%	38	(35.2)	24	(22.9)	38	(33.3)	100	(30.6)	0.239
10%–50%	68	(63)	76	(72.4)	73	(64)	217	(66.4)
$>$ 50%	2	(1.9)	5	(4.8)	3	(2.6)	10	(3.1)
Fat infiltration left LES
$<$ 10%	41	(38) ${}^{\text{a}}$	25	(23.8) ${}^{\text{b}}$	39	(34.2) ${}^{\text{a}}$	105	(32.1)	0.026
10%–50%	65	(60.2) ${}^{\text{a}}$	73	(69.5) ${}^{\text{a}}$	74	(64.9) ${}^{\text{a}}$	212	(64.8)
$>$ 50%	2	(1.9) ${}^{\text{a}}$	7	(6.7) ${}^{\text{a}}$	1	(0.9) ${}^{\text{a}}$	10	(3.1)

*Chi-square test, LMF: lumbar musculus multifidus, LES: lumbar erector spinae, ${}^{\text{a-a}}$ : The same letter indicates no difference between groups, ${}^{\text{a-b-ab}}$ : Different letters indicate a significant difference between groups.

Table 6

Evaluation of fat infiltration by gender, segments and BMI values

	Gender					Segments							BMI
	Female		Male		$P^{*}$	L3-L4		L4-L5		L5-S1		$P^{*}$	Mean $\pm$ SD		Median (Q1-Q3)		$P^{1}$
Fat infiltration
Rigth LMF
$<$ 10%	51	(25) ${}^{\text{b}}$	54	(43.9) ${}^{\text{a}}$	0.001	69	(63.3) ${}^{\text{a}}$	28	(25.7) ${}^{\text{b}}$	8	(7.3) ${}^{\text{c}}$	$<$ 0.001	26.5	$\pm$ 4,7	26.7	(22.02–30.08)	0.328
10%–50%	150	(73.5) ${}^{\text{b}}$	69	(56.1) ${}^{\text{a}}$		40	(36.7) ${}^{\text{a}}$	81	(74.3) ${}^{\text{b}}$	98	(89.9) ${}^{\text{c}}$		25.8	$\pm$ 4.8	24.7	(21.54–30.96)
$>$ 50%	3	(1.5) ${}^{\text{a}}$	0	(0) ${}^{\text{a}}$		0	(0) ${}^{\text{a}}$	0	(0) ${}^{\text{a}}$	3	(2.8) ${}^{\text{a}}$		24.5	$\pm$ 8	21,6	(19.25–31.62)
Fat infiltration
Left LMF
$<$ 10%	52	(25.5) ${}^{\text{b}}$	58	(47.2) ${}^{\text{a}}$	0.001	75	(68.8) ${}^{\text{a}}$	26	(23.9) ${}^{\text{b}}$	9	(8.3) ${}^{\text{c}}$	$<$ 0.001	26.5	$\pm$ 4.6	27	(21.48–29.32)	0.156
10%–50%	148	(72.5) ${}^{\text{b}}$	65	(52.8) ${}^{\text{a}}$		34	(31.2) ${}^{\text{a}}$	82	(75.2) ${}^{\text{b}}$	97	(89) ${}^{\text{c}}$		25.8	$\pm$ 4.9	24,5	(21.64–32.00)
$>$ 50%	4	(2) ${}^{\text{a}}$	0	(0) ${}^{\text{a}}$		0	(0) ${}^{\text{a}}$	1	(0.9) ${}^{\text{a}}$	3	(2.8) ${}^{\text{a}}$		23	$\pm$ 7.3	20	(21.48–31.62)
Fat infiltration
Rigth LES
$<$ 10%	54	(26.5) ${}^{\text{b}}$	46	(37.4) ${}^{\text{a}}$	0.009	72	(66.1) ${}^{\text{a}}$	22	(20.2) ${}^{\text{b}}$	6	(5.5) ${}^{\text{c}}$	$<$ 0,001	25.7	$\pm$ 4.9	24.5	(21.57–29.86)	0.476
10%–50%	140	(68.6) ${}^{\text{a}}$	77	(62.6) ${}^{\text{a}}$		37	(33.9) ${}^{\text{a}}$	87	(79.8) ${}^{\text{b}}$	93	(85.3) ${}^{\text{b}}$		26.2	$\pm$ 4.8	26.1	(20.64–30.25)
$>$ 50%	10	(4.9) ${}^{\text{b}}$	0	(0) ${}^{\text{a}}$		0	(0) ${}^{\text{a}}$	0	(0) ${}^{\text{a}}$	10	(9.2) ${}^{\text{b}}$		25.3	$\pm$ 5	23.2	(21.64–31.20)
Fat infiltration
Left LES
$<$ 10%	54	(26.5) ${}^{\text{b}}$	51	(41.5) ${}^{\text{a}}$	0.002	73	(67) ${}^{\text{a}}$	25	(22.9) ${}^{\text{b}}$	7	(6.4) ${}^{\text{c}}$	$<$ 0.001	25.8	$\pm$ 4.9	25.7	(21.05–30.03)	0.394
10%–50%	140	(68.6) ${}^{\text{a}}$	72	(58.5) ${}^{\text{a}}$		36	(33) ${}^{\text{a}}$	84	(77.1) ${}^{\text{b}}$	92	(84.4) ${}^{\text{b}}$		26.2	$\pm$ 4.7	25.7	(22.12–31.42)
$>$ 50%	10	(4.9) ${}^{\text{b}}$	0	(0) ${}^{\text{a}}$		0	(0) ${}^{\text{a}}$	0	(0) ${}^{\text{a}}$	10	(9.2) ${}^{\text{b}}$		24.6	$\pm$ 5.6	22.1	(22.62–31.22)

*Chi-square test, LMF: lumbar musculus multifidus, LES: lumbar erector spinae, ${}^{\text{a-b-c}}$ : the same letter indicates no difference between groups, ${}^{\text{a-b-c}}$ : Different letters indicate a significant difference between groups, ${}^{1}$ Kruskal Wallis, BMI (body mass index).

In the comparison of the CSA and TCSA values according to age groups, the right and left LES CSA and left TCSA values were found to be related to age ( $p=$ 0.028, $p=$ 0.001, $p=$ 0.002, respectively) (Table 2). In the evaluations of the correlations with age within each group, a weak negative correlation was determined in the healthy control group between age and the left LES CSA and the left LMF $+$ LES TCSA (Table 4). In the mechanical LBP group, there was found to be a weak-moderate correlation between age and the right-left LES CSA and the right-left LMF $+$ LES TCSA values (Table 4). No significant correlation was determined with age in the herniated disc group (Table 4).

In the comparisons of the CSA and TCSA values of the groups according to BMI, a positive correlation was determined between BMI and the CSA and TCSA values of all muscles ( $p=$ 0.021, $p=$ 0.001, $p<$ 0.001, respectively) (Table 2). In the healthy control group, a weak positive correlation was detrermined between BMI and the left LMF CSA and the left LMF $+$ LES TCSA. In the mechanical LBP group, a significant positive correlation was found with all measurements. In the herniated disc group, a weak positive correlation was determined between BMI and the right LES CSA (Table 4).

No significant correlations were determined between the duration of LBP and the CSA and TCSA values (Table 4). In the mechanical LBP group, there was determined to be a significant negative weak-moderate correlation between the VAS resting score and right-left LMF and left LES CSA, and the right-left LMF $+$ LES TCSA values. A significant negative weak-moderate correlation was determined between the VAS activity score and right-left LMF CSA, and the right-left LMF $+$ LES TCSA values. No significant correlation with VAS scores was determined in the herniated disc group.

The duration of LBP was not seen to be different between the groups ( $p=$ 0.737). The median VAS values at rest and during activity were determined to be different between the groups ( $p=$ 0.022, $p=$ 0.006, respectively). The median VAS value at rest was 1 in the mechanical LBP group and 2 in the LDH group. The VAS values during activity were determined as 3 in the mechanical LBP group and 4 in the LDH group.

3.2 Examination of fat infiltration of the groups

In the examinations of fat infiltration according to the groups, significant differences were determined between the right-left LMF and left LES groups ( $p=$ 0.007, $p<$ 0.001, $p=$ 0.026, respectively) (Table 5). The rate of fat infiltration $<$ 10% was determined to be higher in the healthy control group than in the mechanical LBP group and in the herniated disc group, and the rates of 10–50% and $>$ 50% fat infiltration were higher in the mechanical LBP group and the herniated disc group than in the healthy control group.

Fat infiltration in the lumbar paraspinal muscles was observed at a higher rate in females than in males (Table 6). The distributions of right-left LMF ( $p=$ 0.001) and right-left LES fat infiltration showed a significant difference according to gender ( $p=$ 0.009, $p=$ 0.002).

Fat infiltration according to segments (L3-L4, L4-L5, L5-S1) showed a significant difference ( $p<$ 0.001) (Table 6). Fat infiltration in the right-left LMF and LES was seen at the lowest level in L3-L4, and at the highest level in L5-S1. No statistically significant correlation was determined between BMI and fat infiltration ( $p>$ 0.05) (Table 6).

No significant correlation was determined between the duration of LBP, VAS resting and activity scores, and the LMF and LES fat infiiltration (Table 7). In the mechanical LBP group, a positive weak correlation was determined between the VAS resting score and left LMF fat infiltration, but not to a statistically significant level ( $p=$ 0.290). In the herniated disc group, a positive weak correlation was determined between the duration of LBP, and right-left LMF and right-left LES fat infiltration, but not to a statistically significant level, ( $p=$ 0.251, $p=$ 0.263, $p=$ 0.238, $p=$ 0.253, respectively). No statistically significant correlation was determined between age and fat infiltration ( $p>$ 0.05).

Table 7
Evaluation of the relationship between pain duration and severity of pain and fat infiltration

	LBP duration	VAS rest	VAS activity
Mechanical group
Right LMF	$-$ 0.012	0.197	0.126
Left LMF	$-$ 0.231	0.290	0.126
Right LES	0.107	0.144	0.130
Left LES	0.040	0.184	0.126
Herniated disc group
Right LMF	0.251	0.112	0.026
Left LMF	0.263	$-$ 0.026	$-$ 0.100
Right LES	0.238	$-$ 0.058	$-$ 0.161
Left LES	0.253	0.046	$-$ 0.048

LMF: lumbar musculus multifidus, LES: lumbar erector spinae, LBP: Low back pain, VAS: Visual Analog Scale.

4. Discussion

The results of this study did not determine a consistent correlation between LBP and the CSA and TCSA of the LMF and LES. Measurement of the morphology of the lumbar paraspinal muscles has become a focus point of recent research related to the etiology of LBP [2, 8, 18, 19, 31, 53, 54]. It has been suggested that dysfunction of these muscles is an important factor in the etiology of LBP and in it becoming chronic [19, 53]. Previous studies have shown an association between paraspinal muscle atrophy and LBP [2, 18, 19, 28, 31, 32, 52, 55] and fat infiltration [19, 20, 53, 56, 57, 58, 59]. Some of these studies have reported that in chronic LBP there is atrophy only in the LMF and there is no change in the LES [18, 55, 60, 61], some have shown atrophy in both the LMF and LES [19], some have reported a smaller CSA of the LMF, psoas, and quadratus lumborum [52], and others have found no difference in the CSA of either the LMF and LES [25, 62, 63, 64]. Moreover, several researchers have reported that compared to healthy individuals there are no significant differences in the dimensions of paraspinal muscles [35, 58, 59, 65, 66, 67, 68] or fat content [18, 31, 53].

In the current study, the CSA and TCSA values of the LMF and LES obtained in the healthy control group were lower than those of the mechanical LBP and herniated disc groups. This was thought to be due to the pseudohypertrophy mechanism. The CSA basically represents the total number of muscle fibres with, to a lesser degree, the dimensions of the fibres [28] and fat content of the muscle [32]. Dystrophic muscles may not decrease the muscle measurement, and this phenomenon is stated as pseudohypertrophy of fat deposits localised within the muscle fibres [19]. In LBP, impaired neuromuscular function may cause histological changes in the muscle and thereby, atrophy [20]. However, the muscle CSA may decrease not because of fat infiltration formed in the muscle bundles [49]. Muscle density is a marker of muscle degeneration, and represents the number of muscle fibres, the individual muscle fibre area, and the integrity of the contraction material [69]. In the current study, the amount of muscle seen visually on the axial slices of the mechanical LBP goup and the herniated disc group was lower than in the healthy control group, and the fat infiltration was greater, both visually and statistically in the two LBP groups compared to the healthy control group. In individuals with chronic LBP, despite the reduced functional CSA (FCSA) in muscles, the pseudohypertrophy mechanism can be assumed to be a reason for no change or an increase in CSA associated with the rate of increasing fat infiltration. Therefore, to determine whether there is actual loss of mass in the muscles, and hence express muscle degeneration, it can be considered that the examination of FCSA rather than CSA or TCSA is important to be able to obtain correct results, and this was thought to be the reason that no significant correlation was determined in the current study betweeen LBP and the CSA and TCSA of the LMF and LES.

Previous studies have shown that males have greater CSA and higher paraspinal muscle endurance than females, young individuals have greater muscle density than older individuals, and those of lower body weight have higher paraspinal muscle density than those who are overweight [65]. In the current study, the CSA and TCSA values of males in all groups were found to be higher than those of females [2, 17, 31, 32, 33, 34, 46].

BMI and bodyweight have been stated to be associated with larger muscle CSA [35]. Some authors have determined a significant correlation between BMI and the LMF and LES muscle values and an association of BMI with paraspinal muscle changes [28]. However, there are also studies with results showing no correlaation between BMI and CSA [19, 20, 51]. Kalichman et al. determined a low but statistically significant negative correlation between paraspinal muscle density and BMI, and stated that this correlation was significant in females but not in males [49]. In the current study, a weak moderate level correlation was determined between BMI and CSA and TCSA.

Consistent with the findings in literature, when compared according to segments (L3-L4,L4-L5,L5-S1) the lowest CSA and TCSA values were determined at L3-L4, and the highest at the level of L5-S1 [17, 19, 51, 67, 70, 71, 72, 73].

When literature was examined, most studies were of comparisons of asymmetry between the symptomatic and symptomatic sides with groups of acute, chronic, and with and without root compression pain [17, 31, 72, 73, 74]. The results of previous studies of healthy individuals have shown symmetry of the LMF between sides. Hides et al. examined asymptomatic participants between 1992 and 1994 and showed a difference of 3 $\pm$ 4% between the widest edge and the other side [71]. More recently, Stokes et al. reported this rate to be 7.2%–9.6% at the L4-L5 level compared with the smallest edge [34]. Based on these results, it has been stated that asymmetry of $>$ 10% could be seen as potentially abnormal [46]. In the comparisons of asymmetry in the current study, no significant difference was found between the TCSA values of all groups. This result was thought to be related to the balanced distribution of fat infiltration in paravertebral muscles as the pain was not acute, unilateral or root compression pain in the mechanical LBP and lumbar disc herniation groups.

There are a limited number of studies showing a relationship between the duration of pain and CSA [8] and, similar to the current study, the majority of studies have shown a significant relationship between the duration of pain and CSA [2, 50, 67, 75].

Although fat infiltration seems to be a late stage of muscle degeneration, LMF fat infiltration is commonly and strongly related independently of body composition [20]. In obese individuals, body fat accumulates naturally in the muscles throughout the back muscle system, but does not settle at the level of the last two lumbar vertebrae where spine problems are often seen. That fat infiltration is found in these two problematic areas tends to show that LBP is initiated by muscle changes [49]. There is no clarity in literature about the relationship between fat infiltration and chronic LBP [30, 31, 59]. Some studies have reported a relationship between LBP and fat infiltration only in the LMF [51, 56, 57], some studies have reported a relationship with fat infiltration in both the LMF and LES [2, 20, 56, 58, 59, 65], and there are also studies reporting no relationship with fat infiltration in the LMF and/or LES [34]. In the current study, increased fat infiltration in the LMF was observed in the LBP patients compared to the healthy control group, and no significant increase was observed in the LES. The degeneration seen in the LMF muscle in chronic LBP patients is thought to be due to the anatomy, function, and innervation characteristics of the muscle.

A higher rate of fat infiltration was seen in the lumbar paraspinal muscles of females in the current study compared to males, which was consistent with the literature [20, 23, 36, 49].

The amount of intramuscular fat in the LMF and LES has been shown to be significantly increased in the lower lumbar segments compared to upper lumbar segments [49]. The greater paraspinal muscle atrophy (fat infiltration) seen at L5-S1 compared to L3-L4 may be related to a higher rate of degeneration and spinal pathology occurring at this level. The large angle between L5-S1 levels, and that this is the most mobile level of the spine carrying the greatest weight, greatly increase the stress on the vertebral unit. These factors are the probable reason for the paraspinal muscle changes observed at the related level [28]. Consistent with findings in literature, the current study results showed that the greatest fat infiltration was seen at L5-S1 and the least at L3-L4 [2, 18, 49, 74].

No significant relationship was determined in the current study between LBP duration and severity and fat infiltration of the LMF and LES. In studies of the relationship between fat infiltration and LBP, there is limited evidence that there is no significant relationship between fat infiltration and LBP ongoing for periods of less or more than one year [30]. The results of the current study were consistent with the literature.

The main limitation of this study was the relatively small sample size and wide age range because of the difficulty of finding the same number of participants for three separate groups. However, the number of cases was sufficient according to the power analysis. Future studies with more subjects can allow further subgroups of age. Another limitation could be said to be the absence of histological data which could be compared with the imaging findings in the measurement of muscle mass.

5. Conclusion

The results of this study demonstrated an association between fat infiltration in the LMF and mechanical LBP and lumbar disc herniation. It can be considered that in the evaluation of muscle mass, it would be more appropriate to measure muscle atrophy associated with fat infiltration or FCSA, rather than CSA and TCSA. This may explain the absence of a negative relationship between chronic low back pain and CSA and TCSA. We found no relationship was determined between paraspinal muscle asymmetry and mechanical LBP and lumbar herniated disc with no root compression ongoing for longer than 3 months. A higher rate of fat infiltration was determined in females than in males. Fat infiltration was often seen at the lower lumbar vertebral levels (L4-5, L5-S1) and usually in the muscle area adjoining the vertebral body. A correlation was determined between CSA and TCSA and BMI, but no significant correlation was seen with pain duration and severity.

Funding

No funding was received for this study.

Informed consent

Consent was obtained from all participants prior to participation in the study.

Author contributions

A.Y. and T.Y. designed the study, interpreted the data, and made major contributions to the writing of the article. A.O. managed the study. A.Y. evaluated the suitability of the patients and referred potential participants to the polyclinics. All authors read and approved the final version of the manuscript.

Footnotes

Acknowledgments

The authors would like to thank Radiology Specialist Doctor Kerim Temiz for contributing to the MRI interpretations, technician Halil Ibrahim Efe for performing the MRI scans and the Practice Specialist İbrahim Yeşilyurt for assisting with the adaptation of the MRI device to the study.

Conflict of interest

The authors have no confict of interest to declare.

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Evaluation of the degeneration of the multifidus and erector spinae muscles in patients with low back pain and healthy individuals

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2.1 Participants

2.2.1 Magnetic resonance imaging

3. Results

3.1 Examinations of the CSA and TCSA of the groups

Table 1 Comparisons of the age, gender, BMI, duration of pain and pain severity (VAS score) of the patients according to the groups

Table 7 Evaluation of the relationship between pain duration and severity of pain and fat infiltration

5. Conclusion

Funding

Informed consent

Author contributions

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Comparisons of the age, gender, BMI, duration of pain and pain severity (VAS score) of the patients according to the groups

Table 7
Evaluation of the relationship between pain duration and severity of pain and fat infiltration