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INTRODUCTION
Idiopathic scoliosis (Wajchenberg et al., 2015; Skibinska et al., 2016) usually first appears around the time of puberty, with a different peak age of incidence between sexes. It is mainly manifested as coronal scoliosis, reduced sagittal kyphosis, and three-dimensional malformation of horizontal vertebral rotation (Weinstein et al., 2013), affecting 0.5-3 % of adolescents (Hresko et al., 2013; Zapata et al., 2015). The standing posture of the human body is jointly determined by the spine curve and the pelvis. The pelvis not only serves as the basis of the load carrying capacity of the spine, but also constitutes an important mechanical hub of the human body with the lower lumbar vertebrae. Changes in spinal-pelvic morphology and orientation are one of the causes of idiopathic scoliosis.
Extensive studies have been performed on the relationship between coronal imbalance and spinal-pelvic parameters in adult spinal deformity (Kong et al., 2016).
However, there are few studies comparing spinal-pelvic parameters and sagittal spinal-pelvic morphology between patients with adolescent idiopathic scoliosis (AIS) and normal adolescents. In this regard, this study intends to investigate the changes in and correlation between spinal-pelvic parameters in AIS patients, in order to provide reference data for adolescent spinal orthopedics and provide guidelines for clinical practice to reduce symptoms and improve quality of life (Schwab et al., 2010).
MATERIAL AND METHOD
General information. Thin section X-ray (anterior-posterior and lateral) data were collected for retrospective analysis from patients with Lenke 2 AIS, with a Cobb angle of < 80°, in the Departments of Radiology at the Second Affiliated Hospital of Inner Mongolia Medical University and the Inner Mongolia International Mongolian Medical Hospital from April 2014 to November 2018 (Wang et al., 2017).
All patients were diagnosed by chief physicians of orthopedics and spine surgery at both hospitals. A total of 54 patients were screened and 30 were enrolled, including 13 males and 17 females, aged 12-18 years, with an average of 15. 1 years. The control group was comprised of 30 normal adolescents, including 15 males and 15 females, aged 12-18 years, with an average of 15.2 years. Exclusion criteria: (1) spinal trauma or deformity; (2) a history of spine, pelvis, or other surgery that may affect the spinal-pelvic parameters; (3) pelvic deformity, unequal length of lower limbs, or any condition that may affect measurements; and (4) imaging data indicating significant neurological symptoms and signs.
Imaging measurements. Anteroposterior and lateral X-ray films were taken from all patients in standing position with hands on the lower jaw, eyes looking straight, and hip joints fully extended. Pelvic incidence (PI), sacral slope (SS), pelvic tilt (PT), lumbar lordosis (LL), sacral width (SW), and femoral head- sacrum distance (FH-S) were measured on the lateral radiograph as follows:
(1) PI was measured as the angle between a line perpendicular to the superior endplate of sacrum 1 (S1) at its midpoint and a line connecting this point to the center of the femoral heads. If the femoral heads did not overlap in the radiograph, the midpoint of the line connecting the center of the femoral head was taken as a reference point (Fig. 1).
(2) SS was measured as the angle between the superior endplate of S1 and the horizontal line (Fig. 2).
(3) PT was measured as the angle between the line connecting the midpoint of the superior endplate of S1 and the center of the femoral head and the vertical line (Fig. 3).
(4) LL was measured as the angle between the upper edges of lumbar 1 (L1) and S1 (Fig. 4).
(5) SW was defined as the distance between the lowest points of the sacroiliac joints (Fig. 5).
(6) FH-S was the distance between the center of the femoral heads and the vertical line passing through the posterosuperior corner of S1 (Fig. 6).
Statistical analysis. The above parameters were measured twice by the same examiner, and the mean of two measurements was used. The data were statistically analyzed using SPSS 23. 0. First, descriptive analysis was performed to obtain the maximum, minimum, average, and standard deviation for each sagittal parameter of AIS patients and normal controls. An independent sample t-test was also used to compare each parameter between the two groups (P < 0.05 was considered statistically significant). Second, the effect of sex on the spinal-pelvic parameters of AIS patients was investigated. Finally, Pearson correlation coefficient was used to analyze the bivariate correlation between each parameter (P < 0.05 was considered statistically significant; r = 0-0.1 indicates no correlation; r = 0.1-0.3 indicates a small correlation; r = 0.3-0.5 indicates a medium correlation; and r = 0.5-1 indicates a large correlation).
RESULTS
General information. The age of subjects ranged from 12 to 18 years, with an average of (15.24±1.92) years. The AIS group included 30 patients (13 males and 17 females), with an average age of 15.14 years. The control group included 30 healthy subjects (15 males and 15 females), with an average age of 15.33 years.
Sagittal spinal-pelvic parameters and pelvic anatomical parameters of AIS patients and normal controls. LL was measured to be 49.7 ± 8.3°, PI 41.9 ± 9.7°, SS 34.4 ± 8.1°, PT 10.4 ± 4.5°, SW 8.8 ± 0.7°, and FH-S 2.6 ± 1.1° in AIS patients. In normal controls, LL was measured to be 41.3 ± 12.5°, PI 48.7 ± 8.2°, SS 32.1 ± 8.1°, PT 15.8 ± 7.7°, SW 9.4 ± 0.7°, and FH-S 3.4 ± 1.3°. According to the independent sample t-test, PT, SW, and FH-S were significantly lower in AIS patients than in normal controls (all P < 0.05), whereas there was no significant difference in LL, PI, and SS (P > 0.05). It indicates that AIS has a great impact on PT, SW, and FH-S (Table I).
Table I Comparison of spine-pelvic parameters and pelvic anatomical parameters between AIS patients and normal adolescents.
Comparison of spinal-pelvic parameters and pelvic anatomical parameters between sexes in AIS patients. LL was measured to be 47.3 ± 6.9° in male and 51.6 ± 9.9° in female; PI was measured to be 47.7 ± 7.7° in male and 37.3 ± 8.8° in female; SS was measured to be 34.3 ± 7.0° in male and 34.4 ± 9.1° in female; PT was measured to be 12.2 ± 5.5° in male and 9.1 ± 3.2° in female; SW was measured to be 8.7 ± 0.8° in male and 9.0 ± 0.7° in female; and FH-S was measured to be 3.1 ± 1.1° in male and 2.3 ± 1.1° in female. It can be seen that PT was significantly lower in female than in male AIS patients (P < 0.05); in other words, the pelvic parameter, PT, was affected by sex. (Table II).
Table II Comparison of spine-pelvic parameters and pelvic anatomical parameters between different sexes in AISdifferent sexes in AIS.
Correlation between sagittal vertebral-pelvic morphological parameters in AIS patients and normal controls. LL was positively correlated with SS in both AIS patients (r = 0.803, P < 0.05) and normal controls (r = 0.790, P < 0.05). Moreover, in normal controls, PT was linearly correlated with LL (r = -0.557, P = 0.004), PI (r = 0. 416, P = 0. 022), and SS (r = -0. 492, P = 0. 06); and there was also a correlation between PI and SS (r = 0.555, P = 0.01) (Table III).
Table III Correlation coefficient between spine-pelvic parameters of pelvic anatomical parameters of AIS patients and normal adolescents.
** Correlation is significant at the 0. 01 level (2-tailed)
Correlation between spinal-pelvic parameters and pelvic anatomical parameters in AIS patients and normal controls. The anatomical parameter, FH-S, was significantly correlated with the spinal-pelvic parameters, LL, PI, SS, and PT, in AIS patients (all P < 0.05). Moreover, there was a significant correlation between FH-S and PT in normal controls (P < 0.05). It suggests that the horizontal distance between the femoral head and sacrum has a great impact on the spinal-pelvic parameters (Table IV).
DISCUSSION
AIS is a three-dimensional (coronal, sagittal, and transverse) deformity of the spine (Daubs et al., 2013). The spine and the pelvis jointly maintain the balance of the sagittal spinal-pelvic plan to assume an upright posture.
Spinal deformity leads to different degrees of compensatory imbalance of the sagittal spinal-pelvic plane (Ilharreborde et al., 2013), which can easily lead to imbalance of the body’s center of gravity. This may be an important cause of low back pain in adolescents (Spanyer et al., 2015). Surgical treatment can correct the deformity, reconstruct the balance, prevent deformity progression, and significantly improve the quality of life of patients. Preoperative assessment of spinal-pelvic parameters and balance can help to find the least energy-consuming posture and reduce postoperative complications (Crawford et al., 2013).
Spinal-pelvic parameters and anatomical parameters in AIS patients and normal controls. PI is the main axis that controls and regulates the sagittal shape of the spine. Wafa et al., suggested that PI is a fundamental anatomical parameter of the pelvis, which can truly reflect the anatomy of the pelvis, does not change with the position, is not affected by subjective symptoms, and determines the relationship between the pelvis, tibia, and lumbar spine. PI varies with race (Zhu et al., 2014; Banno et al., 2016; Inami et al., 2016) and between individuals. It also changes with individual development. Specifically, PI remains relatively fixed in childhood, increases significantly in adolescence (PI = 0.7436 × age + 39.561° in adolescents older than 10 years), reaches a maximum in adults, and does not change significantly after maturation PI was measured to be 41.9 ± 9.7° in AIS patients with a mean age of 15. 1 ± 2. 0 years, which is lower than 55.5 ± 12.2° measured by Upasani et al. (2007) and 46.70 ± 10.28° (16.21 ± 2.25 years) measured by Ye et al. (2016), but is close to 44.2 ± 10° (14.2 ± 1.6 years) measured by Qiu et al. (Yong et al., 2012). This difference may be related to the age and race of patients. On the other hand, PI was measured to be 48.7 ± 8.2° in normal controls with a mean age of 15. 2 ± 1.9 years, which is higher than 41.1 ± 8.7° measured by Wang et al. (2017), and 41.1°-49.1° measured by Duval-Beaupere et al. (Vaughn & Schwend, 2014). There is a correlation between LL and PI. For example, Legaye et al., suggested that LL ≈ PI + 10° in normal humans, that ideal LL can be roughly estimated based on known PI to obtain the information of global spinal balance, and that PI directly controls SS to increase LL. In idiopathic scoliosis, in order to prevent or limit the imbalance of the sagittal spinal-pelvic plane (Vaughn & Schwend; Aykac et al., 2015), an upright posture is maintained by a compensatory increase in LL or pelvic retroversion.
PT is highly correlated with quality of life. In other words, the rebalance of the sagittal spinal-pelvic plane, especially the return of PT to normal, is critical for quality of life after orthopedic surgery for scoliosis (Wang et al., 2015). It can be seen from Table I that PT was significantly lower in AIS patients than in normal controls (10.4 ± 4.5° for 15.1 ± 2.0 years vs. 15.8 ± 7.7° for 15.2 ± 1.9 years) (P < 0.05). This is consistent with the conclusions of Wang et al. (2009) that the pelvis tilts backwards to compensate for spinal imbalance in patients with spinal deformity and that PT is a measure to evaluate compensation for spinal deformity. The sagittal spinalpelvic plane of AIS patients is characterized by a decrease in PT and pelvic retroversion. In healthy adolescents, the pelvis slightly tilts forward as the body’s center of gravity shifts to the front of the spine due to the upright posture; and at the level of hip joint, the center of gravity should be located behind the hip joint and in front of the second sacral vertebra to counteract the forward tilt caused by gravity. In other words, in healthy adolescents, the sacrum is in a head-down position, the sacroiliac joint is closed, the pelvis and vertebrae are in a neutral position to maintain body balance. By contrast, in AIS patients, the sagittal spine-pelvis plane is out of balance, the sacrum is in a head-up position, and the pelvis tilts backward to maintain body balance.
This study found that an increase in SW increased the stability of the sacroiliac joint, thereby maintaining the spinal-pelvic balance. In AIS patients, SW was significantly lower than that in normal controls, and the sacroiliac joint was not closed, resulting in lumbar lordosis and decreased spinal-pelvic stability. Moreover, FH-S was significantly reduced. The reason for this may be that the acetabulum shifts forward during the pelvic growth, and the pelvis tilts backward as a compensatory response; and consequently, the sacrum is in a head-up position, and the position of the superior sacral endplate changes.
Comparison of spinal-pelvic parameters and pelvic anatomical parameters between sexes in AIS patients. Most studies suggest that there is no significant difference in spinal-pelvic parameters between sexes. However, the progression of AIS is related to puberty. The peak growth period is different between sexess. The growth peak occurs slightly earlier in female than in male. In this study, PT was measured to be 9.1 ± 3.2° in female AIS patients, which is significantly lower than 12.2 ± 5.5° in male (P < 0. 05). This may be related to the difference in the pelvic bone structure between sexes (Schlösser et al., 2014; Giacomini et al., 2015; Bao et al., 2018), a larger anteroposterior diameter of pelvic inlet and wider pubic arch in female, and a higher degree of sacral anteversion in male (Abola et al., 2018).
Correlation between spinal-pelvic parameters in AIS patients and normal controls. In this study, LL was significantly correlated with SS in AIS patients, and LL with SS, PT with LL, and PI with SS, PI and SS in normal controls. This finding is consistent with previous studies. The lumbar vertebrae and sacrum are connected by superior and inferior zygapophyseal joints, ligaments, and muscles. The sacrum is connected to the ilium by the sacroiliac joint and ligaments. Therefore, a tilted sacrum results in the changes of the lumbar vertebrae and pelvis. In other words, SS is positively correlated with LL and PI. It has been demonstrated that PI = PT + SS; that is, a higher PI indicates a tilted pelvis and a higher SS. Previous studies have also found that PI is associated with LL in adult scoliosis. PI can be considered as the core parameter for maintaining the balance of the sagittal spine-pelvis plane. PI was correlated with SS and PT. Specifically, in AIS patients, PI was reduced, and the pelvis tilted backward, which consequently altered the SS and PT, so that more weight was borne by the spinepelvis-lower limb to reduce muscle energy consumption and maintain body balance.
Limitations. First, due to the low incidence of AIS and limited collection time, the sample size was limited, which might induce errors in the spinal-pelvic measurements. Second, only the sagittal spine-pelvis parameters were investigated, whereas coronal and axial parameters were not analyzed. The relationship between the three planes is complicated. Further research is required in this regard. Finally, the results of this study are based on imaging data and need to be validated by long-term follow-up studies.
In summary, PT, SW, and FH-S were significantly lower in AIS patients than in normal controls (all P < 0.05); there was a difference in PT between sexes; LL was positively correlated with SS in AIS patients; LL was positively correlated with SS, PI with SS, PI with LL, and PI with PT in normal controls; and FH-S was positively correlated with LL, PI, SS, and PT in AIS patients. A comparative study of spinal-pelvic parameters between AIS patients and normal controls is instructive for improving quality of life and orthopedic surgery outcomes (Murphy & Mooney 3rd, 2016; Kemppainen et al., 2016; Ohrt-Nissen et al., 2017), establishing sagittal spinalpelvic balance, and maintaining the least energy-consuming posture in patients with AIS.
