The Change of Cervical Spine Alignment Along with BMI in Asymptomatic Population: A Preliminary Analysis

Study design: A cross-sectional study Objective: Methods: This study enrolled 140 asymptomatic volunteers from July 2016 to July 2019. Demographic data included gender, age and BMI, and radiographic parameters included chin–brow vertical angle (CBVA), occipital slope (OS), orbital tilt (OrT), orbital index (OI), occiput-C2 lordosis (O-C2), cervical lordosis (CL), C2-C7 sagittal vertical axis (C2-C7SVA) , cranial tilting (CrT), cervical tilting (CeT), T1 slope (TS), neck tilt (NT), and thoracic inlet angle (TIA). The data were analyzed by ANOVA statistical analyses. inlet lifts in the obese, which can provide clinical advice and remind surgeons of BMI effect in reconstructive surgery for better prognoses. body mass index; CBVA: chin–brow vertical angle; OS: occipital slope; OrT: orbital tilt; OI: orbital index; O-C2: occiput-C2 lordosis; CL: cervical lordosis; C2-C7SVA: C2-C7 sagittal vertical axis; CrT: cranial tilting; CeT: cervical tilting; TS: T1 slope; NT: neck tilt; TIA: thoracic inlet angle.


Introduction
Disruption of cervical sagittal alignment was implicated in the development of various spinal disorders [1][2][3]. And severe cervical sagittal imbalance declined the patient's health-related quality of life [4,5] and even lead to disability through compressing the spinal cord [6,7]. Therefore, cervical sagittal imbalance ought to be attached attention, and factors affecting cervical sagittal balance must be de ned and identi ed before the diagnosis and treatment.
Hence, a number of studies have focused on the factors and the morphology of cervical spine [8,9], and some previous studies [10][11][12] demonstrated cervical sagittal alignment was related to age and gender in asymptomatic population. Meanwhile, obesity was recognized as a global epidemic. In 2015, 600 million adults and 100 million children were obese in 195 countries [13]. Therefore, obese people, who accounted for a large proportion, cannot be ignored. And our previous studies implied that BMI is relative to cervical sagittal alignment [14]. However, there were few studies focusing on the correlation between cervical sagittal alignment and body mass index (BMI), which is a parameter to de ne obesity.
Does cervical sagittal alignment changes as BMI rises in asymptomatic population? Are the standard of diagnosis and treatment different in people with various BMI? To answer these questions, we hypothesized there is a relationship between BMI and cervical sagittal parameters. We grouped asymptomatic volunteers according to different BMI to investigate the correlation of cervical spine alignment changes as BMI rises.

Asymptomatic Population
The institutional review board of the hospital approved this study, and all volunteers approved this study by written informed consent. To begin with, 160 asymptomatic volunteers were recruited from July 2016 to July 2019. During the study, 3 volunteers were excluded due to the history of bony diseases, spinal diseases or myelopathy, 10 volunteers were excluded due to the history of obvious neck or back pain and 2 volunteers dropped out. In addition, 2 radiographs were excluded due to the loss of corresponding demographic data and 3 radiographs were excluded due to the criteria of radiograph. There were totally 140 plain radiographs to explore the correlation between BMI and cervical sagittal alignment.
As for criteria, the inclusion criteria included Cobb angle less than 10° [15,16] in the coronal position, a chin-brow vertical angle (CBVA) less than 10° [9,10,12] in the sagittal position. The exclusion criteria included the history of bony diseases, spinal diseases, or myelopathy, and the history of neck or back pain. In the study, volunteers stood in an erect comfortable position, with elbows fully exed and sts resting on clavicles. Because sts-on-clavicles position was deemed as a more functional sagittal pro le, yielding less negative shift [8]. Radiographs were stored at the Second A liated Hospital and Yuying Children's Hospital of Wenzhou Medical University. The equipment and software used in this study included an AGFA computed radiography system (AGFA Gevaert NV, Mortsel, Belgium), a Siemens 500 mA imaging machine (Siemens Corp., Germany), and a picture archiving and communication system.

Results
Demographic data and radiographic data in asymptomatic volunteers    Fig. 2) In terms of thoracic parameters, we also found signi cant correlations between BMI and parameters.

Discussion
Cervical sagittal imbalance is implicated in the development of various spinal disorders [1,2] and associated with patient's health-related quality of life [4,5]. However, there were few studies focusing on the correlation between BMI and cervical sagittal alignment. After analysis, we derived clear connections between BMI and C2-C7SVA, TZC2-C7, CrT, CeT, CL, NT, TIA (Fig. 2), which indicated that surgeons should take BMI into consideration in reconstructive surgery of cervical sagittal alignment.

Forward Head Posture Increases As Bmi Rises
Several studies [1,9,11,17] testi ed that C2-C7SVA is a crucial parameter in cervical sagittal balance, which was related to clinical symptoms. In study, C2-C7SVA were positive correlated with BMI, which re ected forward head posture increases as BMI rises. In line with our result, Oe et al [9] implied the correlation between C2-C7SVA and BMI in the result of his study. TZC2-C7 is a good addition for C2-C7SVA [18], and we also found TZC2-C7 increases as BMI rises.
CrT is an angle formed by the plumb line and the line connecting the center of T1 upper end plate with the tip of the dens, which is contacted to the exion state of the cervical spine [19]. In study, we found CrT increases as BMI rises, which also re ected the status of forward head posture. Similar to CeT, CeT is also a common parameter to re ect cervical sagittal alignment, and CeT decreases as BMI rises [11,19].
Combining C2-C7SVA, TZC2-C7, CrT, and CeT, we assessed forward head posture increases as BMI rises. This phenomenon may be caused by two reasons. On the one hand, we guessed that the pathological fat in ltration in paraspinal muscle lead to forward head posture. Accumulating evidences demonstrated that BMI was positive associated with fatty in ltration of paraspinal muscle [20][21][22], and previous studies showed that pathological muscle in uences the cervical sagittal alignment [23] and quality of life [24]. On the other hand, the anterior shift of the center of gravity may be an explanation of the compensatory increasement of forward head posture. Accumulating evidences reported that obese individuals have signi cantly greater trunk mass and BMI is positively correlated with increased abdominal fatness [25,26]. And increased abdominal fatness leads to anterior shift of the center of gravity. Previous articles showed that the anterior shift of the center of gravity is compensated with the posterior tilt in the pelvis and the thoracic region [27,28], which explains the anterior tilt in cervical region.
In line with our observed phenomenon, Brink et al. [29] pointed out that overweight or obese students have more neck exion than thinner students, when working on desktop computers in their school computer classroom. And the clinical studies certi ed that obese negatively effect on postural stability, not only in one leg standing but also moving from sit to stand [30,31]; Excessive forward head posture and increased abdominal fatness were regarded as the potential factor of postural instability [32,33].

Thoracic Inlet Lifts As Bmi Rises
As the important element of cervicothoracic junction, thoracic inlet is a circle, made up by T1 vertebral body, rst ribs and the upper part of sternum. As previous studies [34][35][36] described, parameters of thoracic inlet, such as TIA and NT, were signi cant correlative with cervical sagittal balance.
TIA is formed by a line perpendicular to the superior endplate of T1 and a line connecting the center of the T1 upper end plate and the upper end of the sternum. Different from TS, there is no signi cant change of TIA in different positions [37,38], which is an advantage to guide surgery when patients lay, not stand, on the operating table. And TIA was found to markedly increase with age by previous studies [11,12,39], which was consistent with our result. As for BMI, we found there was a correlation between BMI and TIA.
Like TIA, NT is also positively related to BMI, which re ect the phenomenon thoracic inlet lifts as BMI rises, and Oe et al. [9] study also implied that NT was correlative with BMI in the result.
Combining the tender of TIA and NT, we assessed thoracic inlet lifts as BMI rises and the change came from sternum, not T1 vertebral body. We guessed that a rising position of manubrium related to the level of T1 leads to a larger TIA and NT. Shi et al. and Kent et al. certi ed that as BMI rises, the ribs became more perpendicular to the spine and rib cage depth increased, which lead to a rising position of manubrium related to the level of T1 [40,41].
Combining our results with those of previous studies, we assessed that forward head posture increases and thoracic inlet lifts, as BMI rises, in asymptomatic population (Fig. 3). corresponding to our result, Fabris et al [25] showed that postural changes in morbidly obese patients, and Koller et al [42] showed that the risk for revision of adult scoliosis surgery was increased, as BMI rises. Of course, the role of BMI cannot be further exaggerated. Because we found that only signi cant increase of BMI, such as obese, leads to cervical sagittal imbalance, and the cervical sagittal alignment of underweight people is normal. This is the rst preliminary analysis of the change of cervical spine alignment along with BMI in asymptomatic population. In clinic, we advise obese patients with neck pain to lose weight to maintain cervical sagittal balance and reduce neck pressure. In surgery, surgeons can properly evaluate cervical alignment of obese patients with cervical disorders, and map out more precise cervical realignment parameters in obese patient with cervical deformity in infusion operation.
This study has several limitations in fact. First, the number of volunteers can be more to support our conclusions and a larger scale study is our next proposal. Second, our volunteers are all Asians, for which a multi-ethnic study is need in our future. Third, besides sts-on-clavicles position, lying position and sitting position are the next aim.