Lumbar Lordosis Morphology Correlates to Erector Spinae Muscularity in Asymptomatic Asian Adults

Lumbar total lumbar lordosis proximal lumbar lordosis (PLL), distal lumbar lordosis (DLL), lumbar lordosis apex (LLA) and inexion point (IP), evaluated, as well as pelvic incidence (PI) and muscularity of erector spinae (ES) and multidus (MF). Pearson correlation was performed to analyze the relationship between each other parameter. Cases were stratied according to pelvic incidence (very low < 30°, low 30°-45°, moderate 45°-60°, and high > 60°), comparison between groups was performed by univariance analysis.


Results
Strati cation by PI demonstrated PLL increased across groups (p < 0.001), but DLL was comparable between low and moderate PI group (p = 0.329).

Conclusion
Lumbar lordosis morphology correlates to erector spinae muscularity. Proximal lumbar lordosis has a bigger correlation with pelvic incidence than the distal lumbar lordosis. The results are helpful for restoring a rational lumbar lordosis shape in long fusion surgery.

Background
Sagittal spinal alignment and lumbar lordosis shape varies across individuals [1][2][3][4][5] . It has been a research hot spot nowadays, since Roussouly classi cation of normal spinal sagittal pro le 6-8 . Roussouly and colleagues established the classi cation consisting of 5 types according to pelvic incidence (PI) value 8 . Lumbar lordosis (LL) morphology differs among the 5 types, including LL apex, in exion point, LL value, and lordosis distribution index (LDI), which means the proportion of distal lumbar lordosis (DLL) in global lordosis 8 .
Little attention is paid on proximal lumbar lordosis (PLL), until Pesenti and colleagues illustrate the amount of PLL is related to PI 9 , but DLL remains relatively constant. However, the mechanism how LL morphology accommodates to PI has not been deeply investigated, neither the role PLL plays in it.
Paraspinal muscle is supposed a valuable factor in compensatory mechanism of LL morphology, considering it puts an in uence on LL formation in adolescents 10 , as well as on LL degeneration in elderly population [11][12][13] . We retrospectively studied the sagittal pro le and paraspinal muscle condition of 87 asymptomatic young adults, in order to investigate the impact of paraspinal muscle and pelvic incidence on LL morphology and the role of PLL in adjusting LL to them.

Materials And Methods
This was a retrospective comparative study. Between January 2017 and December 2019, 87 asymptomatic adult volunteers were included in the study. All methods were performed in accordance with the relevant guidelines and regulations. Written informed consent was obtained from all subjects participated in the study, and ethical permission to conduct this retrospective study was obtained from the Shandong Provincial Hospital ethics committee.
Inclusion criteria: adult healthy volunteers with age between 18 years and 45 years, without low back pain or radiculopathy symptoms. Exclusion criteria: 1, with spinal deformity; 2, with lumbar or thoracic disease; 3, with hip joint or pelvic disease; 4, with a history of spinal surgery.
Lumbar and pelvic morphology were assessed on lateral 36-inch standing radiographs according to the established positioning protocol (Fig. 1). Pelvic morphology consisted of pelvic incidence (PI), pelvic tilt (PT), and sacral slope (SS). Lumbar morphology included lumbar lordosis (LL), proximal lumbar lordosis (PLL = Cobb angle between L1 and L4 upper endplate), distal lumbar lordosis (DLL = Cobb angle between L4 and S1 upper endplate), lumbar lordosis apex (LLA), and in exion point. The measurement was processed on Surgimap software (Nemaris Inc., NY, US). Lordosis was recorded as negative and kyphosis was recorded as positive.
Erector spinae and multi dus muscularity was de ned as the ratio between cross sectional area (CSA) of erector spinae (ES) and multi dus (MF) and CSA of vertebrae body (VB). The CSA of ES and MF was measured on T2-weighted image by outlining the fascial boundary of the muscle using ImageJ software (National Institutes of Health, Maryland, US). CSA of muscle was calculated as the mean value of bilateral CSA. The measurement of ES, MF and VB was performed at L4 inferior endplate level (Fig. 2), as body weight correlated signi cantly with L4 CSA 14 .
Strati cation by PI value was performed: very low < 30°, low 30°-45°, moderate 45°-60°, and high > 60°, according to the normal distribution of PI in the entire cohort which was tested by Kolmogorov-Smirnov test. Independent t test and one-way ANOVA were performed for comparison of quantitative variables between groups, and Chi square test was performed for qualitative variables. Pearson correlation was performed to analyze the relationship between each other parameter. Linear stepwise regression analysis was also conducted for the relationship between quantitative variables. The distribution of parameters was record as mean and standard deviation. The signi cance threshold was set at 5% (P < 0.05). The statistic calculating was processed on SPSS software (IBM Inc., Chicago, IL, US).

Discussion
Sagittal spinal alignment and lumbar lordosis morphology is highly variable across individuals 1 . A deep understanding of lumbar lordosis morphology is helpful in clinical practice for restoring normal sagittal spinal alignment in long fusion surgeries 9,15,16 . Roussouly and colleagues designed a detailed classi cation of normal sagittal spine pro le in Caucasian population according to PI and SS value 7,8 .
Ethnicity plays an important role in sagittal alignment 17 . Since the entire cohort in the present study was from Asian population, the distribution of Roussouly classi cation was different from previous studies 7 . There were more cases in type 1 (22%, 19/87) and type 2 (32%, 28/87), but less in type 3(33%, 29/87) and type 4(13%, 11/87) in the present study than the previous study 7 .
There was also a different distribution of PI value. Much more cases possessed a PI < 45°, but less with PI > 60° than Caucasian population 8, 9 . It was comparable to Asian population according to previous reports 3,4 . Thus, the cohort was strati ed into 4 groups rather than 3 groups, according to PI value: very low PI group (PI < 30°), low PI group (PI = 30°-45°), moderate PI group (45°-60°), and high PI group (PI > 60°).
Across the strati cation by PI value, not only LL magnitude increases, but also location of LL apex and in exion point migrates higher. The results correspond with the previous studies 5,7,8 . According to the Pearson correlation analysis in the present study, PLL is more variable accommodating to PI than DLL. PLL increases across the groups, but DLL maintains constant between the low PI group and moderate PI group, the majority of the entire cohort (78%, 68/87). It illustrates that PLL plays a more important role than DLL in adjusting LL morphology to PI.
It is also demonstrated by the results of Pearson correlation analysis in the present study. PLL exhibits a correlation with LL apex and in exion joint location, but DLL does not have such a statistically signi cant correlation. It supports the conclusion in Pesenti and colleagues' study that PLL is the driver of compensatory mechanism of LL morphology to PI 9 .
ES muscularity also plays a role in adjusting LL morphology to PI, which is exhibited by the results of Pearson correlation analysis. ES might be one compensatory mechanism of LL morphology accommodating to PI. Several researches in elder patients demonstrate that lumbar muscularity correlates with LL morphology 11,12 . ES muscularity also correlates with the proximal junctional kyphosis (PJK) risk after long fusion surgery 18 . All the results support the assumption above.
The results are helpful for restoring a rational lumbar lordosis shape in long fusion surgery. For a patient with low PI value, a rational LL shape should be restored with a lower LL apex, a smaller PLL, but a same sized DLL, compared to a patient with moderate PI 16 . Otherwise, PJK might occur, because the lower ES muscularity dose not adapt to improper LL shape 18 .

Conclusions
Lumbar lordosis morphology correlates to erector spinae muscularity. Proximal lumbar lordosis has a bigger correlation with pelvic incidence than the distal lumbar lordosis. The results are helpful for restoring a rational lumbar lordosis shape in long fusion surgery.

Declarations
Competing interest disclosure The authors declare no competing interests. The study does not receive funding from any organization.
Ethical approval: Permission to conduct this retrospective study was obtained from the authors' hospital ethics committee.

Consent to participate
All the patients included consent to participate in the retrospective study.

Figure 2
Measurement of cross-sectional area (CSA) of erector spinae (ES) and multi dus (MF) and L4 vertebral body using magnetic resonance imaging. CSA of muscle was calculated as the mean value of bilateral CSA. Muscularity = CSA of muscle -vertebral body ratio.