Analysis of correlation between degeneration of lower lumbar paraspinal muscles and spinopelvic alignment in patients with osteoporotic vertebral compression fracture

Abstract

BACKGROUND:

A few studies have pointed that trunk extensors may affect the spinopelvic alignment; however, little is known about the exact association between degeneration of lower lumbar paraspinal muscles and spinopelvic parameters.

OBJECTIVE:

The study aimed to analyze the relationship between degeneration of lower lumbar paraspinal muscles and spinopelvic alignment in patients with osteoporotic vertebral compression fracture (OVCF).

METHODS:

Thirty-nine OVCF patients were involved in this study. All patients underwent a standing lateral radiographs of the entire spine and pelvis 6 months after kyphoplasty. Pelvic incidence, pelvic tilt, lower lumbar lordosis (LLL) were measured. On the MRI images, the cross-sectional areas of the erector spinae (ES), multifidus (MF), vertebral body and the signal intensity of ES, MF, subcutaneous fat were measured. Pearson’s correlation coefficients was applied to analyze the correlation between the muscular degeneration degree (muscular atrophy and fatty infiltration) and spinopelvic parameters.

RESULTS:

The fatty change degree of ES at L4 inferior endplate level was positively correlated with pelvis retroversion ( $r=$ 0.480, $p<$ 0.05). The grade of fat infiltration of ES plus MF at L5 level was negatively related to LLL ( $r=-$ 0.446, $p<$ 0.05). The fatty change of ES at L5 level, atrophy of ES at L4 and L5 level did not correlate with pelvis back tilt. The fat infiltration of ES plus MF at L4 level, the atrophy degree of ES plus MF at L4 and L5 level had no correlation with LLL.

CONCLUSIONS:

With the increase of fatty infiltration of the erector spinae, the degree of pelvis retroversion increases; the lower lumbar lordosis decreases with the increase of intramuscular adipose tissue of the erector spinae plus multifidus. The atrophy degree of the erector spinae and multifidus is not correlated with pelvis back tilt and lower lumbar lordosis.

Keywords

Lower lumbar paraspinal muscle spinopelvic alignment osteoporotic vertebral compression fracture kyphoplasty

1. Introduction

Osteoporosis with high incidence, especially in the postmenopausal women, is a worldwide health concern [1, 2, 3]. Regional back pain caused by osteoporotic vertebral compression fracture (OVCF) lowers the quality of life in the aging population. Balloon kyphoplasty is identified as a rapid and effective surgical procedure to relieve fracture-associated pain [4, 5, 6], and has a potential to correct local vertebral kyphosis, but could not improve the global sagittal spinal alignment [7]. Thoracolumbar kyphosis accompanied with OVCF is hard to be perfectly corrected by balloon kyphoplasty. For such patients, increasing lower lumbar lordosis (LLL) and pelvis retroversion is the compensatory mechanisms to maintain the whole sagittal balance [8]. In addition, chronic back tiredness is a common complaint of post-kypholasty patients who have difficulty accomplishing activities in which the arms are used in front of the body (e.g., putting away wash basin, ironing clothes). By studying their lumbar magnetic resonance imaging (MRI), it is founded that lower lumber paraspinal muscle, mainly erector spinae (ES) and multifidus (MF), presents varying degrees of fat infiltration and atrophy depending on the individual. And that has been mentioned in other degenerative lumbar diseases [9, 10, 11, 12]. Moreover, LLL and pelvic tilt (PT) vary along with the extent of paraspinal muscle degeneration. ES and MF are the major trunk extensor in the lower lumbar level and their contraction function as stringing the bow to increase LLL. Furthermore, ES plays a significant part in keeping the pelvic anteversion by the means of contraction to pull up the back of the pelvis. No similar studies that had mentioned the exact association between degeneration of lower lumbar paraspinal muscles and spinopelvic parameters in OVCF patients before The purpose of this study is to investigate the correlation between the degeneration grade of lower lumber paraspinal muscles between PT and LLL.

2. Materials and methods

2.1 Subjects

This study retrospected 398 patients with OVCF who initially presented to our clinic for balloon kyphoplasty between March 2011 and January 2015. Inclusion criteria were as follows: (1) Single T12 vertebral compression fracture; (2) Age range from 65 to 75 years old; (3) Patients who can maintain a standing positon after operation; (4) Following up in postoperative 6 months; (5) All patients were operated by the same surgeon. And primary exclusion criteria were as listed below: (1) Pathological fracture caused by metastatic tumor and spine infection; (2) Lumbar disc herniation, spondylolisthesis and stenosis with radiculopathy symptom; (3) Degenerative scoliosis; (4) More than 3 months after fracture. Patients with ankylosing spondylitis; neuromuscular diseases; flat-back syndrome; clinical or history signs of hip, pelvic or lower limbs; previous spine surgery were also excluded. Finally, 39 patients (27 females and 12 males) were included.

Figure 1.

A standard 36-inch digital standing lateral radiograph of a 69 year-old woman with T12 vertebral compression fracture 6 months after kyphoplasty. PT pelvic tilt, PI pelvic incidence, LLL lower lumbar lordosis.

Figure 2.

Measurement of SI and CSA. A, ES at the L4 inferior endplate level: “A 614.6 mm ${}^{2}$ ” is the value of CSA of ES, “Average 294.1” is the mean value of SI of ES, “A 2021.1 mm ${}^{2}$ ” is the value of CSA of VB, “Average 670.9” is the mean value of SI of Fat. B, ES at the L5 level. C, ES plus MF at the L4 level. D, ES plus MF at the L5 level.

2.2 Data collection and image analysis

All patients included underwent a standard 36-inch digital standing lateral and anterior-posterior radiographs of the entire spine and pelvis 6 months after kyphoplasty. Standing lateral radiographs were taken with arms in the fists-on-clavicles position and knees and hips fully extended [13, 14]. The spinopelvic parameters below were measured (using Digimizer Image Analysis software) on the lateral radiographs as described by Lamartina et al. and Jackson et al. [8, 15]: angle between the superior endplate of L4 and the superior endplate of S1 using Cobb method (Lower Lumbar lordosis LLL); angle between a line perpendicular to the sacral plate and a line joining the sacral plate to the axis of the femoral heads (pelvic incidence PI); angle formed by a line drawn from the midpoint of the sacral endplate to the center of the bicoxofemoral axis and vertical plumb line (pelvic tilt PT) (Fig. 1). PI is not affected by the posture or the pelvis position and considered as changeless for a subject after blastocolysis. However, the orientation of pelvis is defined by two positional parameters: the PT and the sacral slope. Barrey et al. defined 6 classes of PI in 154 healthy asymptomatic volunteers from I to VI, and each class of PI possessed the corresponding PT value [16]. To decrease bias caused by individual factors, pelvis retroversion (also called pelvis back tilt) degree was evaluated the ratio of PT to PI multiplied by 100% (PT/PI $\times$ 100%).

Lumbar MRI was performed used Siemens 3.0 T Magnetom vision on the same day with the radiographs. The picture archiving and communication system (PACS) was applied to analyze the T2-weighted axial images at the inferior endplate of L4 and L5 on the right side. On the endplate levels the contour line of ES and ES plus MF was separately constructed by polygon points around the outer edge of the muscles and then the values (mean and standard deviation) of the cross-sectional area (CSA) and signal intensity (SI) of an individual myofiber were available. Using the same method, the CSA of vertebral body (VB) and the SI of subcutaneous fat at the same level could also be obtained (Fig. 2). And all the mean values above were calculated. In order to reduce the error of measuring, 3 authors were involved in the measurement, and the mean values of the data obtained by the 3 authors were used to analyze. For fear of bias caused by individual body size, the degree of muscle atrophia was evaluated by the muscle-VB CSA ratio multiplied by 100% (Muscle/VB CSA $\times$ 100%). In order to reduce bias resulted from differences in the SI of fat between individuals, the grade of fatty change was assessed by the muscle-subcutaneous fat ratio multiplied by 100% (Muscle/Fat SI $\times$ 100%). Above mentioned methods were referred to in the study of Hyun et al. [9]. The interrater reliability and test-retest reliability were demonstrated high levels [17, 18, 19].

SPSS 17.0 package software was used for all statistical analysis. The correlation between the degree of muscular degeneration and spinopelvic parameters was analyzed by Pearson’s correlation coefficients. Statistical significance was set at a level of $P<$ 0.05.

Figure 3.

Positive linear correlation between L4 ES/Fat SI $\times$ 100% and PT/PI $\times$ 100%.

Figure 4.

Negative linear correlation between L5 (ES $+$ MF)/Fat SI $\times$ 100% and LLL.

Table 1

Correlations between the degree (mean $\pm$ SD) of fatty change and atrophy of ES and PT/PI $\times$ 100% (mean $\pm$ SD)

	L4 ES/Fat	L5 ES/Fat	L4 ES/VB	L5 ES/VB
	SI $\times$ 100% (%)	SI $\times$ 100% (%)	CSA $\times$ 100% (%)	CSA $\times$ 100% (%)
PT/PI $\times$ 100% (%) (43.4 $\pm$ 13.0)	49.5 $\pm$ 11.7	58.6 $\pm$ 12.7	83.9 $\pm$ 22.5	48.6 $\pm$ 17.4
$r$	0.480	$-$ 0.068	$-$ 0.228	$-$ 0.283
$p$	0.002*	0.731	0.242	0.145

* $p<$ 0.05. PT pelvic tilt, PI pelvic incidence, ES erector spinae, VB vertebral body, SI signal intensity, CSA cross-sectional area.

Table 2

Correlations between the degree (mean $\pm$ SD) of fatty change and atrophy of ES plus MF and LLL (mean $\pm$ SD)

	L4 (ES $+$ MF)/Fat	L5 (ES $+$ MF)/Fat	L4 (ES $+$ MF)/VB	L5 (ES $+$ MF)/VB
	SI $\times$ 100% (%)	SI $\times$ 100% (%)	CSA $\times$ 100% (%)	CSA $\times$ 100% (%)
LLL ( ${}^{\circ}$ ) (36.9 $\pm$ 8.2)	48.5 $\pm$ 12.4	57.6 $\pm$ 15.2	127.4 $\pm$ 31.6	106.9 $\pm$ 35.0
$r$	$-$ 0.207	$-$ 0.446	0.146	0.167
$p$	0.290	0.004*	0.459	0.379

* $p<$ 0.05. LLL lower lumbar lordosis, ES erector spinae, MF multifidus, VB vertebral body, SI signal intensity, CSA cross-sectional area.

3. Results

Correlations between the grade of fatty change and atrophy of ES at L4 and L5 inferior endplate level (L4 ES/Fat SI $\times$ 100%, L5 ES/Fat SI $\times$ 100%, L4 ES/VB CSA $\times$ 100% and L5 ES/VB CSA $\times$ 100%) and PT/PI $\times$ 100% were analyzed. L4 ES/Fat SI $\times$ 100% was positively correlated with PT/PI $\times$ 100% ( $r=$ 0.480, $p<$ 0.05) (Fig. 3), whereas L5 ES/Fat SI $\times$ 100% did not correlated with PT/PI $\times$ 100% ( $r=-$ 0.068, $p=$ 0.731). L4 ES/VB CSA $\times$ 100% and L5 ES/VB CSA $\times$ 100% also did not correlate with PT/PI $\times$ 100% ( $r=-$ 0.228, $p=$ 0.242; $r=-$ 0.283, $p=$ 0.145) (Table 1).

Correlations between the degradation of ES plus MF at L4 and L5 inferior endplate level (L4 (ES $+$ MF)/Fat SI $\times$ 100%, L5 (ES $+$ MF)/Fat SI $\times$ 100%, L4 (ES $+$ MF)/VB CSA $\times$ 100% and L5 (ES $+$ MF)/VB CSA $\times$ 100%) and LLL were analysed. L5 (ES $+$ MF)/Fat SI $\times$ 100% was negatively related to LLL ( $r=-$ 0.446, $p<$ 0.05) (Fig. 4), nevertheless L4 (ES $+$ MF)/Fat SI $\times$ 100% had no obvious correlations with LLL ( $r=-$ 0.207, $p=$ 0.290). L4 (ES $+$ MF)/VB CSA $\times$ 100% and L5 (ES $+$ MF)/VB CSA $\times$ 100% had no apparent correlation with LLL ( $r=$ 0.146, $p=$ 0.459; $r=$ 0.167, $p=$ 0.379) (Table 2).

4. Discussion

Two important results can be concluded: along with the increase of fatty infiltration of ES at the L4 level, PT increases; with the increase of intramuscular adipose tissue of ES $+$ MF at the L5 level, LLL decreases.

Sagittal alignment was a hot topic in the past two decades, and Glassman et al. advocated that for any reconstructive spine surgery restoration of normal sagittal alignment is the critical goal [20]. It counts for much to reestablish the spinopelvic harmony to obtain satisfactory therapeutic results after surgery as assessed by ODI and HRQOL [21]. But the influence of the degeneration of paraspinal muscle on spinopelvic alignment was currently disregarded.

Positive linear correlation between L4 ES/Fat SI $\times$ 100% and PT/PI $\times$ 100% was found in present study, and it indicated that along with the increase of the degree of fatty infiltration in ES at the L4 inferior endplate level, the degree of pelvis back tilt would also increase. However, at the L5 level this correlation had not been observed. The possible reason may be that the lower extreme of ES is close to L5 level and the relatively thinner ES plays a minor role in keeping the pelvic forward tilt. Likewise, there was no correlation between the atrophy of ES and pelvis retroversion. As for the exact reason, further research is needed.

From the negative linear correlation between L5 (ES $+$ MF)/Fat SI $\times$ 100% and LLL, it could be inferred that LLL tended to decrease following the increase of the degree of fat deposition in ES plus MF at the L5 inferior endplate level. While the relevance did not exist at the L4 level. MF is a vital spinal stabilizer [22, 23, 24, 25] and comprises more than two thirds of the motion of a functional lower lumbar spinal unit [26]. As is well known that MF is smaller on the L4 level than on the L5 level, and that may be the reason for abovementioned two different results. Similarly, the atrophy of ES plus MF had no obvious correlations with LLL. So further research is needed to tease out the specific cause.

Lamartina et al. summarized a classification of sagittal imbalance based on the level of the deformity and pointed out that the subject was not able to keep the normal sagittal alignment with low muscle activity [8]. However, there was no evidence to prove that. If our theory was put into use, that may be explained. Along with the progressive degeneration of ES and MF, LLL decreases and PT increases gradually, and that makes the compensatory mechanism fail in maintaining the whole balance of the spine.

Data indicated that lumbar paraspinal muscle had an effect on spinopelvic alignment in patients with OVCF. Muscles undergo various histological changes, when they degenerate [27], and intramuscular adipose tissue is one important characteristic feature of the changes. The fatty infiltration can be conveniently and rapidly measured using MRI by radiologists and clinicians. Moreover, we wanted to catch the attention of spine surgeons to the importance of degeneration of paraspinal muscles in OVCF patients.

There were several limitations of this study. It was likely to be limited by the low number of enrolled patients and the follow-up period was confined to 6 months after kyphoplasty. If the postoperative follow-up period was extended and a larger amount of subjects were included, the results may be more accurate and reliable. And the effects of spinal ligaments and lumbar intervertebral discs on spinopelvic alignment were not taken account. Moreover, the global sagittal alignment was not under consideration. Furthermore, it was a little bit difficult to define the muscle boundaries exactly on the T2-weighted axial images, especially when the fatty degeneration of paraspinal muscles was severe.

5. Conclusion

Along with the increase of fatty infiltration of erector spinae at the L4 level, the degree of pelvis retroversion increases; with the increase of intramuscular adipose tissue of erector spinae plus multifidus at the L5 level, lower lumbar lordosis decreases. The atrophy of erector spinae and multifidus at the L4-5 level has no correlation with pelvis back tilt and lower lumbar lordosis.

Conflict of interest

None to report.

Footnotes

Acknowledgments

We extend our gratitude to the authors taking part in the study.

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