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 ..In appearance, it is often manifested as body leaning forward instability; whereas on standing full-spine lateral digital radiographs, it shows an increased sagittal vertical axis (SVA) .Clinically, we found that some patients showed normal sagittal balance at initiation, but hunched or leaned forward after a period of walk or activity. This condition is called dynamic sagittal imbalance(DSI). There is no systematic study to explore the paravertebral muscles changes of dynamic sagittal imbalance. Method: The study group comprised 31 DSI patients and 42 control patients. All subjects underwent radiologic whole spine X-ray examination and lumbar MRI( Magnetic Resonance Imaging) scanning. Spinal-pelvic parameters at initiation 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 CSA of the erector spinae (ES), multi ﬁ dus (MF), and vertebral body area were measured at L2/L3 and L4/L5. The fat inltration (FI) and relative cross-sectional area (RCSA)of muscle of these above muscles were quantitatively measured though Image J softwore. Result : Compared with the control group, the DSI group had a smaller lumbar lordosis, more severe fat inltration and lower relative functional cross-sectional area(RFCSA) of paravertebral muscle (erector spinae and multidus) . In DSI group, the point-in-time of occurrence of dynamic sagittal imbalance was statistically correlated with degeneration of paravertbral muscles at L4/L5 level, whereas no correlation between the two above at L2/L3 level. Conclusion:

Clinically, we found that some patients showed normal sagittal balance at initiation, but hunched or leaned forward after a period of walk or activity..Standing full-spine lateral digital radiographs shows increased SVA dynamically. [12]We called this symptom dynamic sagittal imbalance(DSI). These patients often complained marked stooped and leaned forward after a period of activity, without severe lower back pain or neurogenic claudication.Other notable clinical features is as following:1)inability to hold things in front of themselves.2)support with elbows in order to wash dishes or faces.3)di cult in climbing slopes.4) prefered to carry things on their back rather than hold them in front of themselves.
These symptoms are similar to degenerative lumbar kyphosis(LDK),degenerative at back syndrome,drop body syndrome. [21 ] Takemitsu et al. rst introduced "lumbar degenerative kyphosis", which included a marked decreased lumbar lordosis even lumbar kyphosis caused by degenerative changes in elderly people, and Takemitsu classi ed LDK into four types according to the sequence of the spine. [22,23] Degenerative at back syndrome is a subtype of ASD which is rare in western countries.In western countries,it usually caused by iatrogenic factors, such as Harrington rod system surgery .But in Asian countries it is one of the common spinal deformities. [24,25]Zhou XH et al.rencently characterized DSI an normal SVA (SVA 40mm) at initiation,and prominent increase in SVA (SVA≥40mm) after activity with thunks marked inclined,and rstly proposed a quantitative diagnostic criteria and novel classi cation of DSI. [26] Paravertebral muscle has long been viewed an important factor in the stabilization of spinal sequence.Among them, erector spinae and multi dus play important roles in the extension of the spine in reaction to gravity and body weight to maintaining spinal balance. [4] [11]Takemitsu et al. reported pathologic features of LDK as marked paravertebral muscle atrophy with adipose in ltration. [18,22]Although the exact pathophysiology of flat back has not yet been explicated, extensive degeneration of lumbar extensor muscles are thought to be responsible for degenerative at back syndrome in most patients.Drop Body syndrome described by Mitsuru et al. was a primary lumbar kyphosis without obvious coronal deformity, aslo accompanied with severe atrophy and fatty in ltration of the MF muscle. [21]However, there is no systematic study to explore the paravertebral muscles changes of dynamic sagittal imbalance.
.The present study mainly aimed to explore the changes of paravertebral muscles in DSI patients,which would help spinal surgeons better understand the importance of paravertebral muscles in maintaining the balance of spine.

Methods
Demographic characteristics 470 outpatients and inpatients at the Department of Spine of the authors' facility from March 2018 to May 2020 were recruited. All participants were asked to ll in the form 1.For a primary diagnosis of DSI, the patient must meet one major criterion and/or more than one minor criterion .After that,all subjects underwent radiologic whole spine X-ray examination in the natural standing position. Patients with prewalk sagittal vertical axis(SVA) 40mm on imaging were excluded . [12] Then these participants who met the primary diagnosis were asked to participate a 10-minute walk experiment at their usual speed,in order to verify that symptoms of DSI do exist.They were asked to wear tight clothing for easy observation. Dynamic posture images of the entire walk test was obtained using a high-resolution camera , which was placed on a tripod at hip-height. Two well-trained spine surgeon would supervise each partcipant for the entirety of the 10-min walk experiment. Marker points were de ned at anatomic landmarks(C7 and junction of hip), trunk inclination angle (INC)refers to the angle of the junction of hip and C7 marker from the vertical. [32]After that,two well-trained spine surgeon would measures these dynamic posture images , once the partcipant's thunk incline(INC 10°),the point-in-time was recorded.The thunk inclination needed to be con rmed DSI by two spine surgeon togehter. Point-intime was assessed twice by two independent spinal surgeons ,and the average value was calculated as the nal result.Finally, the total of 31 patients was included as the DSI groups. DSI patients could be classi ed into ve subgroups based on the point-in-time:0≤time 2min 2≤time 4min 4≤time 6min 6≤time 8min 8≤time 10min.
.Among the remaining 439 participants , the enrollment criteria of control group include :no history of chronic low back pain (NRS score > 3) or a history of spinal surgery.To reduce bias because of obesity and age, the participants were matched with the DSI patients on the basis of body mass index (BMI) and age ..Finally,A total of 42 people were selected for the control group.Moreover, Numeric Rating Scales (NRS, 0-10) for back pain and Oswestry Disability Index (ODI) scores were routinely collected.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 at initiation. Spinal-pelvic parameters such as pre-walk sagittal vertical axis (pre-walk 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 .MRI was performed using 1.5T Magnetom Vision (Magnetom Symphony; Siemens, Berlin, Germany) scanners. Five T2-weighted 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 [3,13],the muscle fat in ltration(FI) area was estimated using the subcutaneous fat threshold as the standard. 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),divided the FCSA of each muscle by the CSA of the upper endplate of L5. [13]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.
All datas was assessed twice by two independent spinal surgeons ,and the average value was calculated as the nal result.

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 fat in ltration between the DSI group and control group.The correlation between paravetral muscles changes and point-in-time of occurrence of dynamic sagittal imbalance was analyzed by Spearman correlation coe cient,and simple linear regressions were simultaneously conducted. All datas were presented as mean values±SEM (standard error of the mean). P-value<0.05 was considered to be statistically signi cant.

Discussion
Sagittal balance is a primary issue for clinical assessment of spine. [1]The value of SVA has obvious correlation with HRQOL(Health related quality of life).The larger the C7-SVA, the worse the HRQOL.
[2]Sagittal imbalance have always been a concern for spinal surgeons,restoring normal spinal balance is particularly important in the treatment of spinal disorders. [27]Paravertebral muscles have long be considered playing important roles in maintaining spinal stability. [11]Among these paravertebral muscles, erector spinae and multifidus got more attention for their function.Their functions are the extension of the spine in reaction to gravity and body weight as well as the maintainance of lumbar spine stability,the degeneration of paravertebral muscle may cause instability of the spine. [28]In previous study paravertebal muscle changes in different spinal disorders have been extensively studied. [8][9][10]However, there is no systematic study to explore the paravertebral muscles changes of dynamic sagittal imbalance.
Recently,in Zhou's innovative study, 133 adult spinal deformity patients with stooping and back pain after walking were retrospectively analyzed,he aslo proposed a quantitative diagnostic criteria and novel classi cation of DSI. [26]Different from Zhou's study,in present study,any subjects with low back pain (NRS 3)was excluded,in order to minimize the interference of low back pain to the sagittal imbalance.In previous studies,Paul et al. had con emed the decreased lumbar stability in low back pain(LBP) patients,which may lead to sagittal imbalace. [5]In our previous study, we also demonstrated that severe LBP due to lumbar disc herniation can lead to sagittal imbalance in some patients. [6]Therefore, we can't overlook the roles of LBP in sagittal balance.
Moreover,we found that DSI patients had decreased lumbar lordosis compared with patients in control group.Previous studies have demonstrated decreased lumbar lordosis and lumbar kyphosis could cause SVA changes,a decreased lumbar lordosis or lumbar kyphosis is positively correlated with increased SVA.
[4] [7]Many factors may contribute to decreased lumbar lodosis.However, in this cross-sectional study ,it was hard to explore the cause of the reduction in lumbar lordosis, which may require a long-term longitudinal study.
Paravertebral muscle degeneration is characterized by a decrease of muscle size and in ltration of fat tissue,these features predict the deterioration of muscle function. [5] [6]In previous study, Shahidi et al. found there was an increase in fatty in ltration with age in erector and multi dus muscles [29]Fortin et al. conducted a longitudinal study on magnetic resonance imaging of MF muscle for more than 15 years and found that muscle fat in ltration was signi cantly correlated with body mass index (BMI).
[33]Thus,in present study, the control participants were matched with the DSI patients on BMI and age.
As we all know, anterior translation of the gravity line would lead to the fatigue of back extensor muscles, which further accelerates sagittal imbalance [28] [30]. Therefore,in our study, patients with pre-walk SVA 40mm on imaging were excluded there was no statistically signi cant differences in SVA at initiation between the two above groups.We minimized the disturbance of SVA at initiation to the sagittal imbalance,in order to explore the in uence of paravertebral muscle on DSI only.
From our stduy, we found that DSI patients had more severe fat in ltration of paravertebral muscles compared with patients in control group. In preious study [28],Jun et al.noticed that muscle-strengthening exercises could serve to maintain the quality of spinopelvic muscles and thus prevent spinal sagittal imbalance.In Zhou's recent study,they also speculated that the weakening of paraspinal muscles leads to the occurrence of dynamic sagittal imbalance.Thus in our opinion ,beacuse the degeneration of paravertebral muscles is more sever in DSI patients compared with control participants, there were marked differences identi ed at same spinal sequence between the DSI group and control group, with DSI consistently worse with poorer paravertebral muscle function and more prone to fatigue.That's why DSI patients got stooped during the 10-minute walk test. (Fig. 3)Lower extremitiesrelated compensatory mechanisms sagittal imbalance is complicated ,included the exion of knees as well as extension of the hips and ankles. [31] Left the effect of lower extremities not considered,at initiation before the 10-minute walk test, paravertebral muscles in DSI patients were su cient to keep sagittal balance. However,during 10-min walk test, paravertebral muscles get fatigue quickly for reduced endurance and strength of paravertebral muscles.Whereas in control group,paravertebral muscles are strong enough to keep sagittal balance during 10-min walk test. Furthermore,we found the point-in-time of occurrence of dynamic sagittal imbalance was statistically correlated with degeneration of paravertbral muscles at L4/L5 level,whereas no correlation between the two above at L2/L3 level. It was a novel nding that lower lumbar paravertebral muscles play important roles in maintaining spinal balance compared with upper paravertebral muscles.Xia [10] studied the assciation between paravertebral muscles and spinal-pelvic parameters in patients with LDK,they found the the fat in ltration and atrophy of erector spinae at the lower lumbar level would affect the pelvic parameters,which may lead to spianl sgittal imbalance.The PDSI ( Primary degenerative sagittal imbalance) concept has been proposed recently by Chang-hyun Lee , xed sagittal imbalance(SVA 4cm at initiation) with severe paravertbral muscles degeneration. [17]Therefore, We conjecture that DSI is the prestate of PDSI.In DSI patients, although the paravertebral muscles had degenerated to an extent, they could still maintain spinal balance during short periods of activity.Whereas in PDSI patients,as the paravertebral muscles degenerate further, even at the time of motionless standing,they would get fatigue quickly and are unable to maintain sagittal balance.
The present study had some limitations that need further discussion and investigation.First, an inherent limitation of this study is the sample size, which might lead to selection bias.Future work will collect a larger sample to explore the detailed characteristics of DSI patients.Second,because most of the participants were outpatients, we did not use the gait analysis or take post-walk full-spine X-ray photograph to get more detailed differences between pre-walk and post-walk ,because it was inconvenient in the busy outpatients.Third, it is relatively hard to apply our conclusions to relatively young patients,because the average age in the present paper is 63.7±4.8 years.Future work will collect a larger sample to establish baseline values for the change in DSI patients in different age groups and gender groups.Fourth, the compensatory mechanisms of lower extremities has not been taken into account in this study. Full-body radiographs are needed to evaluate the effect of lower limbs in further plan.Fifth, in this cross-sectional study,it is hard to expolre its dynamics of DSI,loneger follow-up of these DSI patients should be collect to explore dynamic change the of DSI.

Conclusions
In conclusion,DSI an normal SVA (SVA 40mm) at initiation,and prominent increase in SVA (SVA≥40mm) after activity with thunks marked inclined.Paravertebral muscle degeneration plays an important role in the DSI process,Patients in the DSI group had more severe paravertebral muscle degeneration compared with patients in control group.There was a signi cant correlation between the severity of DSI symptoms and the degeneration of lower lumbar paravertebral muscles. These ndings may help spinal surgeons better understand sagittal balance of spine. Availability of data and materials All datasets on which the conclusions of the manuscript rely were presented in the main paper.
Competing interests The authors declare that they have no competing interests.
Funding This article did not receive any funding.
Authors' contributions JS and GW thought out the study, participated in its design and coordination. NR carried out this study, did the statistics and drafted the manuscript.XC polsih the manuscript . YL collected part of the data.All authors read and approved the nal manuscript.  For a primary diagnosis of DSI, the patient must meet one major criterion and/or more than one minor criterion .  The values are given as mean±SD. *Statistical significance.
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.