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Lee, Hyun, and Kim: Reciprocal Changes in the Whole-Body Following Realignment Surgery in Adult Spinal Deformity

Abstract

The idea of the global balance of spine stems from Jean Dubousset, who first introduced the concept of cone of economy. Through the compensatory mechanisms, the human body maintains an upright posture and horizontal gaze in the setting of the spinal malalignment. Compensation takes place not only in the mobile spine segments, but also in the pelvis and lower extremities. Patients with a malalignment exhibit compensatory changes in the cervical hyper-lordosis, posterior pelvic shift, knee/ankle flexion, hip extension, and the pelvic retroversion. The advent of whole-body stereo radiography has yielded an improved understanding of global changes among the patients. Deformity-induced compensatory changes in the sagittal alignment could be resolved reciprocally after the surgical correction of the malalignment. Thoracolumbar realignment surgery restores the pathologic compensatory changes in the unfused spinal segments, pelvis, and the lower extremities. Similarly, reciprocal changes in the thoracolumbar spine may harmonize global sagittal alignment after the cervical reconstruction. This study reviews the compensatory mechanisms and reciprocal changes in global sagittal alignment caused by the surgical correction and highlights, the factors that should be considered while assessing a patient’s compensatory status.

Introduction

The idea of the global balance of spine stems from Dubousset [1], who first introduced the concept of the cone of economy (COE). The notion of a sagittal alignment subsequently emerged in the field of the thoracolumbar spine based on the pelvic parameters [2]. Over the last few decades, the importance of the sagittal plane and its contour has gained a significant recognition. The regions of the spine are not independent of each other. The concept of a sagittal alignment regarding the spinopelvic parameters and reciprocal changes in the thoracolumbar spine has been well documented [37]. Spinopelvic balance, described in terms of the reciprocal changes of thoracic kyphosis (TK) and lumbar lordosis (LL) is based on the morphology and orientation of the pelvis. Pelvic incidence (PI) significantly affects the sagittal alignment of the spine, especially LL [810]. In the thoracolumbar spine, the PI minus LL mismatch significantly affects the sagittal imbalance and health-related quality of life (HRQoL) [1117].
With the advent of full-body stereo radiography, our understanding regarding the compensatory mechanisms in the patients with a spinopelvic imbalance has progressed rapidly, and the concept of the reciprocal change has expanded to the field of cervical spine and the lower extremities. During the last decade, correlations of the cervical alignment with a thoracolumbar spine and HRQoL have been researched extensively [1822]. The cervical spine is an adaptive spinal segment regarding a global sagittal alignment (GSA). The PI correlates with LL, LL with TK, and TK with the cervical lordosis (CL) [3]. The chain of correlation between the PI and sagittal parameters are well established. A large PI requires a large LL, which results in an increased TK. An increase in the TK correlates with an increased CL [3]. In the cervical spine, a sequential linkage of correlation of the parameters from T1 slope (T1S) to the cranium has been demonstrated. Small T1S results in a small CL to maintain the physiological neck tilting [23]. The T1S determines the amount of sub axial lordosis required to maintain the head-balance and changes depending on the GSA [3]. The maintenance of a horizontal gaze is an essential function of the upright posture and GSA [24]. Cervical alignment is affected by GSA through the compensatory mechanisms to maintain an upright posture and a horizontal gaze [2428]. In the past, cervical alignment was regarded as a bridge between the cranium and thoracolumbar spine. However, research on the relationship between a cervical alignment and GSA has developed further. This study aims to review the compensatory mechanisms and the reciprocal changes in the whole-body caused by a spinal realignment surgery.

Compensatory Mechanisms in Standing Sagittal Alignment

The sagittal balance reflects the spine’s shape, allowing the individuals to maintain a standing position with a minimal muscle force. Recent investigations have shown that cervical alignment is affected by the GSA through the compensatory mechanisms to maintain an upright posture and a horizontal gaze [2426,2932]. Patients with thoracolumbar malalignment exhibit compensatory changes in the form of cervical hyper-lordosis, posterior pelvic shift, ankle dorsiflexion, knee flexion, hip extension, and the pelvic retroversion [31,3335]. A radiographic analysis of the Scheuermann’s disease showed a cervical hyper-lordosis, a similar compensatory mechanism for the hyperkyphotic thoracic spine [36].
Likewise, changes in cervical kyphosis (CK) reduce TK to correct the alignment and maintain the COE of global spinal balance. Compensation in the CK occurs via a posterior shifting of the C7 sagittal vertical axis (SVA), small T1S, and a large LL [35,37]. Moreover, increased TK causes hyper-lordotic cervical alignment and vice versa [35].
The normal aging process induces the truncal stooping [38]. Several compensatory mechanisms have been implemented to maintain the optimal GSA, including increased CL, PT, ankle flexion, and the knee flexion (Fig. 1) [3941]. The aging-related deterioration of the GSA is compensated by supportive functions of the spine, pelvis, and the lower limbs [30]. The reciprocal changes from the thoracolumbar to the cervical spine, and lower extremities occur in a staged fashion to maintain a horizontal gaze and global balance [41]. Roussouly and Pinheiro-Franco [42] hypothesized the following sequential mechanism of the compensation of progressive kyphosis: (1) a normal stage with the slight pelvic retroversion and the C7 plumb line (PL) over the sacral endplate, (2) a compensated stage with a progressive loss of LL and the pelvic retroversion to maintain the C7 PL behind the femoral heads, and (3) a decompensated stage, wherein hip extension limits the pelvic retroversion, which is compensated by a knee flexion, and the C7 PL passes forward to the femoral heads. With the hips maximally extended and the knees flexed, the last posture is well known in severe kyphosis, and it is very uncomfortable and uneconomical [42]. Therefore, it is necessary to evaluate the GSA, particularly in older patients with a cervical spondylotic myelopathy, because of their compensatory mechanism for the global malalignment [43].

The Era of Whole-Body Imaging

A new X-ray imaging system, the EOS system (EOS imaging, Paris, France), was developed by the interdisciplinary investigators to overcome the limitations of a conventional radiography. Using a three-dimensional bone external envelope technique, EOS allows bilateral long-length images (whole-body or localized) in either the standing or seated position, with the overall enhanced image quality, and lower radiation dose for the patient [44,45]. Obtaining a whole-body image in a single scan provides a full-scale image without a vertical distortion, improving the accuracy of the surgical planning measurements.
The advent of whole-body radiographs has led to a better understanding of the reciprocal changes in the cervical spine and the lower extremities in patients with the horacolumbar deformities. Using the EOS imaging system, the normal location of the bony landmarks in standing whole-body radiographs in reference to the gravity line (GL) has been reported (Fig. 2) [30]. The mean value of the offset distance from GL to the center of the acoustic meatus was 0, and this value was not affected by the aging [30]. With the age, the L4 and L5 vertebrae and sacrum shifted posteriorly. Loss of lordosis and an increase in the PT were induced by the posterior shift of the lower lumbar vertebrae and the sacrum, maintaining an optimal positioning of the GL [30].
Previous studies have been reported that the measurements made using an EOS lateral whole-body stereo-radiographs showed an equivalent reliability to those obtained by using the conventional cervical lateral radiographs [46]. EOS resulted in the lower measurements for C2−7 SVA (0.68 cm lower) and C1−7 SVA (1.02 cm lower) than the conventional X-rays, with significant differences between the groups. However, there were no differences in the C2−7 lordosis, T1S, neck tilt, or the thoracic inlet angle [46].
Unlike the conventional radiographs, the EOS imaging system presents the information on the alignment of the spine and lower extremities, emphasizing the significance of a full-body analysis to comprehend the patient’s status. Without a detailed analysis of the lower extremities, the spine cannot be evaluated properly. The key to understand the sagittal balance is detecting the imbalance, severity, and diagnosing combined problems involving the lower extremities [41,47]. The compensatory mechanisms implemented to maintain an optimal GSA also occur in the lower extremities, including the hip extension, knee flexion, and the ankle dorsiflexion [30,41]. Accordingly, all the elements of the chain of balance considered to evaluate the static global balance [41]. However, it is difficult to use the conventional radiographs to assess the lower extremities or head position [39]. Therefore, using the preoperative EOS evaluation aids full-body analysis of a patient, leading to an optimal preoperative planning.

Reciprocal Changes from the Thoracolumbar to the Cervical Spine

Patients with a thoracolumbar malalignment exhibit compensatory changes in the form of cervical hyper-lordosis, posterior pelvic shift, ankle dorsiflexion, knee flexion, hip extension, and the pelvic retroversion [33,34]. Maligned patients showed a larger CL, Sacro-femoral, and knee flexion angles than the well-aligned patients [34]. These compensatory mechanisms resolve reciprocally in a linear fashion following the optimal surgical correction of malalignment [29,33].
Correction of the thoracolumbar malalignment has been shown to result in a reciprocal change in the adjacent thoracolumbar regions [4851]. Pedicle subtraction osteotomy (PSO) of the thoracic or lumbar spine results in a reciprocal change (decreased TK in the lumbar PSO, decreased LL in the thoracic PSO) [48]. Protopsaltis et al. [50] reported that the reciprocal TK could be predicted in preoperative planning, and the surgeon should consider the extent of the surgical instrumentation accordingly. After the correction of a sagittal thoracic deformity, the lordotic compensatory mechanisms occur at the closest mobile curve by decreasing the LL, especially in the lower thoracic deformity [51].
Multiple studies have been reported about the reciprocal changes in the cervical alignment ensuing surgical correction of thoracolumbar deformity over a last decade [26,29,33,34,5154]. Thoracolumbar realignment surgery restores the pathologic compensatory mechanisms in the unfused spinal segments and the lower extremities, especially in patients fused from the upper thoracic spine [34,51]. Similarly, after a thoracolumbar arthrodesis, changes in the TK and LL were significantly associated with a CL. Reciprocal change in the T1S and C2−7 SVA were associated with the selection of the upper instrumented vertebra (UIV). If the UIV was in the lower thoracic spine (T9 or lower), reciprocal changes were not observed, whereas if the UIV was in the upper thoracic spine (T1−8), there were significant reciprocal changes [54]. The spontaneous correction of the CK is due to the restoration of TK and reciprocal changes between the cervical and thoracic spine.
Ha et al. [26] reported that the changes in the CL after a deformity correction were correlated with the magnitude of the sagittal deformity. The high C7 SVA group showed a decreased CL, postoperatively; whereas, in the lower C7 SVA group, CL significantly increased after a thoracolumbar deformity correction [26].

Reciprocal Changes from the Cervical to the Thoracolumbar Spine

The primary goal of the cervical reconstruction surgery is to achieve an occiput-trunk concordance [55]. Occiput-trunk discordance is defined as a distance over 30 mm between the GL and C7 PL [56]. Once occiput-trunk concordance is achieved, the subsequent thoracolumbar alignment changes occur as needed to harmonize the GSA, showing that the cervical reconstruction may restore both cervical deformities and GSA [55].
A few studies have analyzed the compensatory mechanism of the CK and reciprocal changes after the CK correction [37,55,5759]. Mizutani et al. [55] thoroughly investigated the reciprocal changes on radiographs after the correction of cervical deformities. They classified the patients into two CK groups according to the preoperative C7 PL location (Fig. 3). The head-balanced patients were those with the negative SVA values, hyper-LL, and a low T1S. Trunk-balanced patients had positive SVA values, upper-limit PI-LL values, and a normal T1S. Subsequently, thoracolumbar alignment changed to harmonize the entire spinal alignment. Correction in the head-balanced group resulted in the anterior shifting of C7 PL, a subsequent increase in the T1S and TK, and a decrease in the LL.
Reciprocal changes after the correction of CK suggest that the patients exhibit different patterns depending on whether they have an adequate compensatory capacity in the thoracolumbar spine. In our practice, we divide the patients into two CK subgroups (Fig. 4). In patients with a compensated CK (i.e., head-balanced) (Fig. 4A, B), the posteriorly shifted C7 PL before the surgery moves anteriorly after a correction. Subsequently, TK and T1S increase while the LL decreases. In contrast, no significant changes in thoracolumbar alignment occur in the patients with a decompensated CK (i.e., trunk-balanced) (Fig. 4C, D) following a surgical correction. In a previous study of these two groups, patients with a decompensated CK decreased in the T1S and TK, but no changes occurred in the spinopelvic and lower extremity parameters. In addition, the C0–1 and C1–2 angles became kyphotic and less lordotic, after the surgery [57]. No changes were observed in the pelvic and lower extremity parameters in both the groups [57]. As specific implications, selective cervical correction would be possible for the compensated subtype, whereas both the cervical and thoracic correction would be necessary for the decompensated subtype [57].

Relationship between HRQoL and Sagittal Alignment

It has been reported that aging affects the HRQoL with a deteriorating sagittal alignment [60]. With an increasing age, spinopelvic mismatch increases in a normal population, resulting in the higher Oswestry Disability Index (ODI) score, suggesting that the spinopelvic malalignment correlates with a poor HRQoL in an aging population due to a spinopelvic mismatch [40].
Likewise, the severity of disability increases with a positive global malalignment in both cervical and thoracolumbar spine following the surgical correction of the deformity [11,57,61]. The C7 SVA is a vital parameter regarding the GSA. The C7 PL significantly correlates with the HRQoL [11]. The normal C7 SVA should be <5 cm, but the parameter is age-dependent [62]. Any pathology interfering with the equilibrium instigates a sagittal malalignment resulting in the significant change in HRQoL. Even the mild imbalance is detrimental, and a linear correlation of the HRQoL and sagittal imbalance has been demonstrated [11].
In the thoracolumbar spine, the spinopelvic mismatch significantly affects the sagittal imbalance and HRQoL [1113]. Higher grades of the spinopelvic mismatch significantly correlate with the poorer HRQoL [12]. Combining spinopelvic mismatch with the C7 SVA provides a guideline in patient assessment and in the therapeutic decision-making [13]. The correlation between the ODI score and compensatory mechanisms of the pelvis and the lower extremities has been shown [41]. Changes in the regional cervical sagittal parameters correlate with the HRQoL in patients, and improvement in the regional cervical alignment improves the HRQoL [28]. The C2−7 SVA and T1S–CL are correlated with the multiple measures of HRQoL [22,63,64]. The C2−7 SVA is positively correlated with the Neck Disability Index (NDI) scores [22,28,61,65]. In addition, T1S–CL is correlated positively with the C2–7 SVA and NDI scores [65]. Achieving operative goals, including the proper GSA or cervical alignment, maximal correction of the focal kyphosis, and correcting the horizontal gaze leads to the optimal HRQoL [66].

Discussion

The study provides a comprehensive background material on the compensatory mechanism of the spine after the reconstructive surgery. The association between a cervical alignment and GSA has not been thoroughly investigated. The cervical alignment adjusts to maintain an upright posture and a horizontal gaze through the compensatory mechanisms of the GSA [1016]. In CK patients, the C7 SVA shifts posteriorly, T1S decreases, and the LL increases to compensate the GSA [20,23]. LL influences TK and has only an indirect effect on the cervical alignment [43]. Similarly, compensation in the thoracolumbar malalignment patients occurs through a cervical hyper-lordosis, posterior pelvic shift, knee flexion, hip extension, and the pelvic retroversion [1820].
Adults with a spinal deformity and positive sagittal malalignment compensate with an abnormally increased CL to maintain their horizontal gaze, and correction of the sagittal malalignment results in the correction of the abnormal cervical hyper-lordosis through the reciprocal changes. Patients who achieved full correction of the positive sagittal malalignment had the greatest relaxation of cervical hyper-lordosis [15]. Changes in the CL after a deformity correction are correlated with the magnitude of the sagittal deformity [26]. Patients show different patterns of reciprocal changes after the cervical deformity correction depending on the compensatory capacity of the thoracolumbar spine [57].
Therefore, assessing the whole-body alignment rather than the whole-spine images is necessary to understand patients’ GSA and their compensatory status thoroughly. Previous reports regarding a cervical deformity did not take GSA into account, and instead focused only on the local parameters.
The normal locations of the bony landmarks in standing whole-body radiographs in reference to the GL using the EOS imaging system have been reported [30]. The mean value of offset distance from the GL to the center of an acoustic meatus was 0, and this value was not affected by the aging [30]. Accordingly, reconstruction surgery aims to achieve the occiput-trunk concordance by positioning the center of the gravity above the femoral heads [34].
Achieving the optimal alignment leads to potential improvements in the clinical outcomes. The patient’s degree of disability rises with a positive global malalignment following the surgical correction of a deformity [8,36,39]. Cervical alignment parameters such as: C2–7 SVA and T1S–CL are positively correlated with the HRQoL [22,61,63,65]. Achieving the proper GSA, cervical alignment, maximal correction of focal kyphosis, and correcting the horizontal gaze could lead to optimal HRQoL [42]. Therefore, future research on the surgical correction of the sagittal malalignment should focus on the compensatory status of the patient’s GSA to provide an ideal correction. Furthermore, the active use of the whole-body stereo radiography is highly recommended, as the results measured by the EOS lateral whole-body stereo radiography show results with a comparable reliability to those obtained using conventional cervical lateral radiographs [29].

Conclusions

Understanding of compensatory mechanisms among the spine, pelvis, and lower extremities is mandatory for treating the spinal deformity. These compensatory mechanisms could be evaluated using a whole-body imaging. The proverb, “Do not miss the forest for the trees.” is helpful to understand a malalignment of the spine. A meticulous preoperative evaluation of the whole-body alignment, including the pelvis and lower extremities, is paramount to appreciate the optimal GSA in the correction of spinal malalignment.

Conflicts of interest

Conflict of Interest

No potential conflict of interest relevant to this article was reported.

Fig. 1
(A) Whole-body image of thoracolumbar malalignment exhibits cervical hyperlordosis, posterior pelvic shift, and knee flexion. (B) Postoperative whole-body image of the same patient exhibits restoration of lumbar lordosis (from 1.6° to 65.2°) with reciprocal changes of thoracic kyphosis (from −4.9° to 37.2°), cervical lordosis (from 23.1° to 9.5°), pelvic tilt (from 33.1° to 12.3°), knee flexion (from 9.5° to 3.6°), and ankle dorsiflexion (from 7.4° to 0.7°).
asj-2021-0451f1.jpg
Fig. 2
Normative offset distances between bony landmarks and the gravity line. Positive values denote locations anterior to the gravity line and negative values indicate locations posterior to the gravity line. CAM, center of the acoustic meatus, CI, confidence interval.
asj-2021-0451f2.jpg
Fig. 3
Compensatory mechanisms in patients with symptomatic cervical kyphosis. PL, plumb line; CK, cervical kyphosis; LL, lumbar lordosis; PI, pelvic incidence; TK, thoracic kyphosis.
asj-2021-0451f3.jpg
Fig. 4
A representative case of a patient with cervical kyphosis. Preoperative and postoperative wholebody stereoradiographs showing the center of gravity (COG) plumb line (PL) (blue line) and C7 PL (red line). (A) A preoperative clinical picture of a compensated cervical kyphosis patient. Hyperlordotic thoracolumbar compensation resulted in skin redundancy and a crease in the lumbar spine (yellow arrow). (B) Compensated cervical kyphosis patient with the COG PL located on the femoral head, but the C7 PL located markedly posteriorly. Cervical malalignment was corrected to achieve global sagittal balance and occiput-trunk (OT) concordance. However, the lowerextremity alignment parameters did not change significantly. (C) Clinical picture of a decompensated cervical kyphosis patient. (D) Decompensated cervical kyphosis patient with the COG PL located markedly anteriorly, but the C7 PL located on the femoral head. Sagittal PLs indicated cervical sagittal imbalance and OT discordance before surgery. No significant changes were found in lumbopelvic alignment or the lowerextremity alignment parameters. T1S, T1 slope; TK, thoracic kyphosis; LL, lumbar lordosis; PI, pelvic incidence; SFA, sacrofemoral angle; KA, knee angle; AA, ankle angle.
asj-2021-0451f4.jpg

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