Moderate Degeneration of the Lumbar Paravertebral Muscle in Patients With Dynamic Sagittal Imbalance,A retrospective cohort study

Study Design: A retrospective cohort study. Background: Sagittal imbalance of the spine is a comprehensive concept and can be caused by many causes. Paravertebral muscle is an important factor in the stabilization of spine.The active subsystem formed by the muscles around the lumbar spine plays an important role in maintaining lumbar spine stability and extendding the spine . Clinically, we found that some patients showed spinal sagittal balance when they were energetic, but hunched or leaning forward after a period of walking or working.Standing full-spine lateral digital radiographs shows increased sagittal vertical axis (SVA)dynamically.We call this symptoms a dynamic sagittal imbalance (cid:0) DSI. However, the sagittal sequence, paravertebral muscle changes, and the correlation between them in DSI patients have not been clearly explored. The purpose of this study was to investigate the changes of spinal-pelvic parameters; paravertebral muscle; and the relationship between the two in DSI patients . Method: The study group comprised 31 patients with DSI and 42 control patients.All subjects underwent radiologic whole spine X-ray examination and lumbar MRI( Magnetic Resonance Imaging) scanning. Spinal-pelvic parameters such as sagittal vertical axis (SVA), thoracic kyphosis (TK), thoracolumbar kyphosis (TLK), lumbar lordosis (LL), sacral slope (SS), pelvic tilt (PT) and pelvic incidence (PI) was measured. The cross-sectional areas (cid:0) CSA (cid:0) of the erector spinae (ES),multi ﬁ dus (MF), and vertebral body were measured at L2/L3 and L4/L5. The fat inltration (FI) and relative cross-sectional area (RCSA)of muscle of these muscles were quantitatively measured though Image J. All subjects were examined for bone mineral density and pulmonary function to test the overall skeletal muscle capacity. Result: Compared with the control group,the DSI group had a smaller lumbar lordosis (cid:0) more severe fat inltration and lower Relative functional cross-sectional area(RFCSA) of paravertebral muscle ES(erector

pathophysiology of flat back has not yet been explicated, extensive degeneration of lumbar extensor muscles are thought to be responsible for the syndrome in most patients.Drop Body syndrome described by Mitsuru et al. was a primary lumbar kyphosis without obvious coronal deformity, accompanied by severe atrophy of the MF muscle and fatty in ltration. [34]Different from the deformity of the spine structure described above (1. PI-LL> 40°;2.LLK >-10 °;3.Slight deformity of the coronal plane), as well as the obvious sagittal imbalance in the natural standing position (SVA > 5cm or SVA > 10cm), [35,37,40]we found that DSI patients often presented a balanced sagittal plane in the resting position without obvious spinal deformity.
However, there is no systematic study to explore the pathophysiological mechanism of dynamic spinal sagittal imbalance.The Spinal-pelvic parameters, the changes of paravertebral muscles, whether there is a correlation between the two above, and whether there is a degeneration of the systemic muscle capacity of individuals, have not been systematically elucidated.

Method
Demographic characteristics 470 outpatients and inpatients at the Department of Spine of the authors' facility from March 2018 to May 2020 were recruited.VAS and ODI scores were routinely collected.Any Participants with ankylosing spondylitis, spinal arthrodesis, post-traumatic kyphosis or compression fractures, and neuromuscular disease are excluded.Participants wereasked to ll in the form 1.For a diagnosis of DSI, the patient must meet one major criterion and/or more than one minor criterion .Finally, the total of 31 patients was included as the DSI groups.Among the remaining 438 Participants ,Control subjects included in this group had no history of chronic low back pain (VAS score > 3) , a history of neurogenic claudication and a history of spinal surgery,Finally,A total of 42 people were selected for the control group.This study protocol was approved by the Ethics Committee of our institution .

Spinal-pelvic parameters
All subjects underwent radiologic whole spine X-ray examination in the natural standing position. Spinal-pelvic parameters such as sagittal vertical axis (SVA), thoracic kyphosis (TK), thoracolumbar kyphosis (TLK), lumbar lordosis (LL), sacral slope (SS), pelvic tilt (PT) and pelvic incidence (PI) was measured. Lordosis was de ned negative and kyphosis was de ned positive . The method of measuring the angle is Cobb method.

Paravertebral muscle evaluation
All subjects underwent MRI( Magnetic Resonance Imaging) examination of lumbar area .Magnetic resonance imaging was performed using 1.5T Magnetom Vision(Magnetom Symphony; Siemens, Berlin, Germany)scanners. Five T2-weighted(Repetition time/ echo time=3,500-3,600/112-120 ms ) axial images from L1/L2 to L5/S1 level were obtained from MRI. Paravetebral muscles were evaluated from the center slice of each of the 5 images.
The scale was marked in the original T2-weighted axial images,then images were imported into Image J (Version1.52a.National Institutes of Health.USA) for analysis.Four regions of interest (ROI) for the muscles were manually de ned at the center slice of each of the 5 images: the ROI for the multi dus, the erector spinae muscle were de ned bilaterally. Total CSA (cross-sectional area) was estimated.According to the method proposed by Ranson and Seung-Jae Hyun [3,25],the muscle fat in ltration(FI) area was estimated using the subcutaneous fat threshold as the standard. (Fig.2)Then the functional CSA (FCSA, lean muscle) of each muscle was calculated by Total CSA minus the fat in ltration area.In order to compensate for the bias of individual relative body size to muscle CSA, we calculated relative CSA (RCSA)(25), i.e.dividing the each muscle FCSA by the CSA of the upper endplate of L5.The fat in ltration rate(FI) ,RTCSA( Relative total cross-sectional area )RFCSA (Relative functional cross-sectional area )of each muscle at L2/L3 level and L4/L5 level was calculated.Each image was assessed twice by two independent spinal surgeons ,and the average value was calculated as the nal result.
Bone mineral density (BMD)test and pulmonary function test (PFT) All subjects were examined for bone mineral density and pulmonary function in order to test the skeletal muscle capacity of the whole body. [27]Bone mineral density was measured at the lumbar spine and left femoral neck by dual-energy X-ray absorptiometry (DEXA, GE Medical Systems Lunar). The BMD of the left femoral neck of the patient was selected for comparison.PFTs were measured with a computerized spirometer with an accuracy of ± 3%. The absolute peak expiratory ow (PEF) and percent-predicted values (ppPEF) were assessed for each participant.The American Lung Association (ALA) scale was used to categorize ppPEFs into the following zones: green(normal), ppPEF > 80%; yellow(mild decline), 50-79%; red(severe decline ), < 50%. [26] Statistical Analysis Statistical analysis was performed using the Statistical Package for Social Science (SPSS Inc., Chicago, IL), Version 12.0. The Mann-Whitney U test was used to assess for differences in the demographic data,the Relative total CSA, Relative functional CSA and the rate of fat in ltration between the DSI groups and control groups. The correlation between individual muscle degeneration at L2/L3 and L4/L5 level and spinalpelvic parameters in DSI groups and control groups was analyzed by Spearman correlation test independently.ALL the data is presented as mean values±SEM (standard error of the mean). P-value<0.05 was considered to be statistically signi cant.

Result
Demographic data The DSI group comprised 3 man and 28 women (age, 64.1±5.1 yo; height, 159.8±6.3cm;and BMI, 25.0±3.3). The control group comprised 2 man and 40 women (age, 60.8±5.3y; height, 158.3±6.4cm; and BMI, 23.9± 3.4). There were no significant differences in age, body weight, height, or BMI between the 2 groups ( Table 1). The DSI group ranging from 1.25 years to 28 years 9.8±7.5y had a longer history of low back pain than the control group ranging from 0.3 years to 20 years 4.8±5.0y . However, there were statistically signi cant differences in age and history of low back pain between the two above groups. (Table. 2)

Spinal-pelvic parameters
There were no significant differences in TK ,TLK,PT,PI,SS or SVA between two groups. However, there were statistically signi cant differences in LL between the two above groups. The DSI group ranging from -37.9 to 36.1 -6.5±24.1 had a lower LL than the control group ranging from -55.6 to 21.7 -22.4±20.5 (Table.3 (Table.5) The skeletal muscle capacity of the whole body There were no significant differences in BMD of left femoral neck between the DSI group(0.827±0.126) and the control group(0.836±0.132). (Table.2) PFT results for DSI patients indicated that the PEF and ppPEF were in the green range in 51%, the yellow range in 45% and the only one(3%) were in the red range (mean 527 ± 126L/min and 79 ± 18%).PFT results for 42 control group patients showed that the PEF and ppPEF were in the green (normal) range in 60%(green), the yellow range (mild decline) in 38% and the red range in 2%. (mean 519 ± 96 L/min and 80 ± 14%). There were no significant differences in PEF,ppPEF between two groups. (Table.2)

Correlation analysis
Correlation analysis was conducted between the FI,RTCSA,,RFCSA of multi dus, erector spinae, and the spinal-pelvic parameters in the DSI group.Finally it was con rmed that there was no correlation between muscle degeneration and Spinal-pelvic parameters in both DSI group. (

Discussion
Sagittal balance is a primary issue for clinical assessment of spine. [1]The larger the C7-SVA, the worse the HRQOL(Health related quality of life). [2]Skeletal structure and paravertebral muscles of spine play an important role in maintaining spinal stability.Among them, ES and MF of lumbar spine were considered important in paravertebral muscles [20]Their function is the extension of the spine in reaction to gravity and body weight as well as the maintainance of lumbar spine stability,degeneration of them can cause instability of the spine. [4]Paravertebral muscles degeneration is characterized by a decrease of muscle size and in ltration of fat tissue. [5,6] This study described a common clinical symptom and investigated its demographic characteristics, spinal-pelvic parameters, and paravertebral muscle degeneration.

Demographic characteristics
In present study, the DSI group was older and had a longer history of low back pain than the control group.
Many factors contribute to the tendency of older people to sagittal imbalance.LG Lenke et al. described increasing age correlated to a more forward sagittal vertical axis with loss of distal lumbar lordosis [7]. Paul S Sung con rmed the stability index of the spine signi cantly decreased during low back pain a trunk muscle imbalance may contribute to unbalanced posture.In our previous study, we also demonstrated that severe low back pain due to lumbar disc herniation can lead to sagittal imbalance in some patients, and a decrease in the EMG activity of the lumbar paravertebral muscles can be founded. [8,9] In this study, The VAS score of both the DSI group and the control group was controlled under 3 score, and there was no statistical difference .We do not believe that the symptoms of DSI are caused by low back pain.

Spinal-pelvic parameters
In present study, the DSI group had a smaller lumbar lordosis than the control group, with no statistically signi cant difference in other Spinalpelvic parameters(such as TK ,TLK,PT,PI,SS). Different from the previous research Jee-Soo Jang , Bae J S et,al. demonstrated that the change of thoracic kyphosis,thoracolumbar (T-L) junction angle ,spinal-pelvic parameters play important roles in compensating the sagittal imbalance in LDK patients. [10,11]Many factors could cause lumbar kyphosis, such as muscle degeneration, disc degeneration,post-laminectomy iatrogenic kyphosis, and vertebral fracture. [12,13]However, in present study ,it was di cult to explore the cause of the reduction in lumbar lordosis, which may require a long-term longitudinal study.When lumbar lordosis is reduced or lumbar kyphosis occurs, overwork of the lumbar extensor muscles is required to maintain spinal balance. [14]Therefore, in the DSI group, even in the natural standing position, paravertebral muscles are more prone to fatigue,which lead to the sagittal imbalance.

Paravertebral muscle degeneration
Paravertebral degeneration is characterized by a decrease of muscle size and in ltration of fat tissue.In previous studies, degeneration of lumbar paraviral muscles can be caused by multiple factors, such as low back pain, lumbar disc herniation, spinal stenosis, and changes in spinal structure. [15][16][17][18]In this study, we found that the paravertebral muscle MF ES degeneration in the DSI group, and the paravertebral muscle degeneration in the L4/L5 level was seriously changed.Our conclusion is consistent with that of Weiwei Xia et,al.
[18]The possible reasons we think are as following:1)two thirds of the lumbar lordosis are located at the last two lumbar levels L4S1 = 0.66 × L1S1 [19].Thus, in patients with reduced lumbar lordosis, more morphological changes were present in the L4-S1 lower lumbar spine.L4-S1 segmental kyphosis elongates paravertebral muscles and exacerbates their dysfunction,which leads to the degeneration of paravertebral muscle at L4/L5 level .2)The paravertebral muscle in lumbar kyphosis has a shorter lever arm length than in lordosis, which may lead to a decreased movement of the lumbar spine.It may lead to disuse atrophy of the paravertebral muscles. [20] 3)Kaan Yaltirik et al. had proved that long-term pressure on the root caused by disc herniation can cause atrophy and degeneration of that muscle group. [17]About 70% of lumbar disc herniation occur in L4/L5 level.In degenerative lumbar diseases, there are usually multiple levels of intervertebral disc herniation or spinal canal stenosis. [14]Therefore, paravertebral muscle degeneration in DSI patients is caused by multiple factors.

The skeletal muscle capacity of whole body
The PFT results and BMD results were all comparable in patients with the DSI and the control.It showed no difference in overall musculoskeletal capacity between the DSI and the control group.Sarcopenia is de ned as an age-related decline decline in skeletal muscle mass,usually accompanied by a decrease in bone mineral density. [22]The PFT results in the both groups were even larger than those of the age-matched and sex-matched healthy Chinese volunteers described by Zhong NS et al,which suggesting normal muscle capacity in both patients. [23]These suggests isolated degeneration of the lumbar paravertebral muscles in the DSI group.It is similar to Drop Head Symptoms and Drop Body Symptoms.Both accompanied by segmental kyphosis and severe degeneration of the local extensor muscles. [35,40] The reason of the DSI The Drop Body Symptoms described by Mitsuru Yagi presents a xed sagittal imbalance(SVA 10cm accompanied with severe isolated paravertebral muscle degeneration. [35,40]Camptocomia is de ned as an involuntary exion of the throcolumar spine ,without xed kyphosis ,which increase during standing and walking ,and abate in the supine position.Camptocomia can be caused by many reasons,paravertebral muscle degeneration is an important cause. [34]Kalichman divided paravertebral muscle degeneration into three levels: Grade 1, normal ( 10% fat in ltration);Grade 2, moderate muscle degeneration( 10%-50% fat in ltration);Grade 3, severe muscle degeneration( 50% fat in ltration). [21]Severe FI of lumbar paravertebral muscle was found in both Drop Body and Camptocormia. [34,35]Drop Body and Camptocomia consistently showed immediate leaning forward even when patients were energetic.The DSI tends to lean forward after a period of walking or manual labor.In present study ,it can be seen that the fat in ltration rates of L2/L3 level (MF:41.2%±10.3% ES:30.6%±9.6%) and L4/L5 level (MF:49.6%±12.3% ES:34.4%±7.4%) in the DSI group, which was far lower than those described by Drop body and Camptocomia(MF ES: 80% . Takemitsu also described that in LDK patients, some patients had leaning forward when they were exhausted, but there was no speci c study on the degree of paravertebral muscle degeneration. [14] Chang-hyun Lee proposed one concept called PDSI ( Primary degenerative sagittal imbalance. [4]The diagnosis for PDSI must meeting the following criteria :(1.C7-SVA ≥5 cm, 2.pelvic incidence -lumbar lordosis ≥15°, 3. pelvic tilt ≥25°,4.paravertebral muscle degeneration,5.Symptoms of spine sagittal imbalance. )Some primary imbalance (such as LDK,Flat back syndrome ,Drop body syndrome were categorized into this concept. [4] Different from the diagnosis of PDSI, which both imaging diagnosis and clinical symptom diagnosis are required.We focus more on the diagnosis of clinical symptoms.Different from the severe paravertebral degeneration in PDSI patients,DSI have only moderate paravertebral muscle degeneration. The paravertebral muscle degeneration is caused by multiple factors.The function of DSI patients paravertebral muscle was better than that of PDSI patients.When the DSI patient is energetic, the degenerative paravertebral muscles can be actively activated to maintain spinal balance. When paravertebral muscles are fatigue (walking or moving for a period of time), it is di cult to maintain sagittal balance of the spine, resulting in forward leaning or hunchback.And as the lumbar lordosis decreases, the paravertebral muscles need to do more work to maintain spinal balance.Theoretically, patients with reduced lumbar lordosis are more likely to develop DSI symptoms at the same degree of muscle degeneration as compared to normal sagittal sequence.However, severe DSI symptoms can occur even in people with normal sagittal sequence (Fig.3).And as the paravertebral muscle continues to degenerate to a severe degree,even in energetic state, the paravertebral muscles of the lumbar spine are not strong enough to maintain sagittal balance,which leads to a marked leaning forward posture,that is PDSI.There have been no studies to investigate the synergy between lumbar sequence and degenerative paravertebral muscles in patients with sagittal imbalance.Therefore we believe that the DSI described in this study is actually the pre-state of PDSI. (Fig.4).
The study also has some limitations.1)This study may be limited by the small number of patients enrolled.The reason is the low incidence of DSI, which may require more studies based on a large population of multicenter studies.2)The radiologic whole spine X-ray was lacked when the DSI patient was exhausted .The changes of sagittal plane sequence before and after the patient's imbalance have not been explored in detail.Junseok Bae had assessed global and regional spinal sagittal radiographic parameters in adults with loss of lumbar lordosis (" atback") before and after walking 10 minutes,LL PT TK has its related compensation mechanism,but the paravertebral muscle changes have not been described. [15]3 There is no speci c method to quantify the severity of symptoms in DSI patients, so we did not explore the correlation between the severity of symptoms and paravertebral muscle degeneration, sagittal plane sequence in DSI patients.

Conclusion
In conclusion,DSI is the pre-state of PDSI, along with moderate degeneration of the paravertebral muscles of the lumbar spine.Usually accompanied by a reduction in lumbar lordosis.A DSI patient is usually characterized by a balanced sagittal sequence when he is energetic, and a gradual forward leaning posture when he is exhausted.As paravertebral muscle continue to degenerate, the DSI may be transformed into a xed sagittal imbalance.Early diagnosis of DSI and relevant intervention may effectively reverse and delay the occurrence of xed sagittal imbalance.
Competing interests The authors declare that they have no competing interests.
Funding This article did not receive any funding.
Authors' contributions JS thought out the study, participated in its design and coordination. NR carried out this study, did the statistics and drafted the manuscript.GW and XC polsih the manuscript . YL collected part of the data.All authors read and approved the nal manuscript.
Acknowledgements The authors would like to thank Dr.Binghao Bian and Dr. Jianlong Li for the assistance in collecting cases .  4. Support with elbows in order to wash dishs or face? YES/NO For a diagnosis of DSI, the patient must meet one major criterion and/or more than one minor criterion . The values are given as mean±SD.
A P-value of 0.05 was considered to indicate statistical signi cance . The values are given as mean±SD.
A P-value of 0.05 was considered to indicate statistical signi cance . A P-value of <0.05 was considered to indicate statistical significance. A P-value of <0.05 was considered to indicate statistical significance.