Introduction

The significance of sagittal balance in preoperative assessments of spinopelvic profile, influencing both surgical planning and procedure, is increasingly recognized [1]. Values for sagittal parameters of the spine vary significantly depending on age and population.

Proper understanding of spinal sagittal balance parameters is critical as it has been shown to correlate with health-related quality of life [2]. Sacral slope, pelvic tilt, and pelvic incidence are used to depict the shape and orientation of the pelvis, whereas cervical lordosis, thoracic kyphosis, and lumbar lordosis constitute sagittal alignment of the whole spine [3]. Pelvic incidence is closely related to the shape of the lumbar spine, as evidenced by several formulas that use mismatched values between pelvic incidence and lumbar lordosis to predict ideal lumbar sagittal alignment [4]. Cervical lordosis is known to be influenced by C7 or T1 slope and cSVA, which are key determining factors of cervical sagittal alignment [5].

The sagittal alignment of the spine and pelvis in children differs from that in adults. Sagittal alignment patterns also change with age [6]. The aim of the surgical procedure is to make the maximal correction on the coronal and transverse planes and to restore the physiological curves on the sagittal plane. Prerequisite for sagittal plane reconstruction is to know the physiological values. Understanding the spinopelvic sagittal balance in healthy children is crucial to a deeper understanding of the pathological state of spinal pathologies and the physiological reconstruction of physiological curvature during surgery.

Some studies have reported the complications of cervical spine imbalance after instrumental surgery for AIS [7]. However, few studies have reported normal values for spinopelvic sagittal balance parameters, including cervical spine parameters, in large samples. Thus, the aim of the present observational study is to examine the parameters of sagittal alignment of the regional spine and spinopelvic region in asymptomatic pediatric populations and the characteristics of these parameters with age and sex.

Methods

Study population

This study involves healthy pediatric individuals of the Han Chinese ethnicity in China who sought medical evaluation at the Spinal Surgery Outpatient Department of the Third Hospital of Hebei Medical University between January 2022 and July 2023 for screening of “scoliosis.” All participants, aged between 4 and 15 years, underwent whole-length EOS examination in the standard standing protocol to rule out spinal deformities. Ethical approval and consent to participate this study was approved by the ethics committee of the Third Hospital of Hebei Medical University. All patients and their guardians were fully informed about the clinical trial and the legal guardians of patients had signed the informed consent to participate.

Inclusion criteria for this study encompass individuals who, following both thorough clinical physical examinations and imaging studies, exhibit no discernible evidence of scoliosis. Following a detailed explanation of the study’s objectives to the patient and guardian, consent was granted for the utilization of imaging data within this research. Conversely, exclusion criteria are applied to individuals presenting with evident scoliosis or congenital developmental anomalies, including but not limited to hemivertebrae, butterfly vertebrae, and spinal segmentation disorders. Individuals with a documented history of spinal trauma or infection are excluded from participation in this study. Patients with pelvic or lower limb abnormalities or deformities are excluded from the study. These stringent criteria ensure a focused and homogeneous study cohort. For the analyze trends in spinal sagittal alignment, participants were categorized into three age-based cohorts: 4–7 years (Group A), 8–11 years (Group B), and 12–15 years (Group C).

Radiology and measurements

All patients underwent a standardized radiographic protocol, assuming a comfortable standing position with shoulders and elbows positioned in front of the body. All data were saved, extracted, and measured through the picture archiving and communication systems (PACS). Risser sign was also assessed on anteroposterior EOS radiographs.

The detailed measurement methods of the parameters are as follows:

Cervical parameters (Shown in Fig. 1A): T1 Slope (T1S) and C7 Slope (C7S) measure the inclination of the upper thoracic spine and C7 vertebra, respectively. The Cervical Sagittal Vertical Axis (cSVA) is the distance from a plumb line through the C2 center to the posterior upper endplate of C7. The C2–7 Cobb angle is calculated from perpendicular lines drawn from the inferior endplates of C2 and C7.

Fig. 1
figure 1

A Demonstrates the measurement schematic of the cervical sagittal vertical axis (cSVA), The C2–7 Cobb angle, T1 slope (T1S) and C7 slope (C7S). B Demonstrates the measurement schematic of thoracic kyphosis (TK). C Demonstrates the measurement schematic of lordosis (LL), pelvic incidence (PI), pelvic tilt (PT) and sacral slope (SS)

Full size image

Thoracic and lumbar parameters (Shown in Fig. 1B): Lordosis (LL) and Thoracic Kyphosis (TK) are measured from the superior endplates of L1 to S1 for LL, and T5–T12 for TK, using the Cobb method.

Pelvic parameters (Shown in Fig. 1C): Pelvic Incidence (PI) is defined by the angle between a line perpendicular to the sacral plate's midpoint and a line to the femoral heads’ axis. Pelvic Tilt (PT) is the angle from the vertical to a line from the sacral plate's midpoint to the femoral heads’ axis, reflecting pelvic orientation. Sacral Slope (SS) is the angle between the horizontal and the sacral plate, indicating sacral endplate inclination.

Evaluation of intra-rater and inter-rater reliability

Three spine surgeons conducted radiographic measurements utilizing the PACS software. To evaluate intra-rater reliability, each rater measured all radiographic parameters a second time, with an interval of 2–3 weeks following the initial assessment. Throughout the evaluation period for inter-rater reliability, each rater remained unaware of the measurements made by the other. The measurement reliability was assessed through intraclass correlation coefficients (ICCs). Intra- and interobserver ICCs for estimating the spinopelvic sagittal parameters were 0.83 and 0.85, suggesting high reliability of these measurements using these three observers.

Statistical analyses

The data were analyzed using SPSS software (version 24; SPSS, Inc., Chicago, IL). The Shapiro–Wilk test was employed to assess the normality of distribution for each parameter within the dataset. For parameters conforming to a normal distribution, independent sample t-tests were conducted. Conversely, for parameters not adhering to a normal distribution, the Mann–Whitney U test was utilized for comparing spinopelvic parameters between boys and girls. Descriptive statistics are presented as mean ± standard deviation. The chi-square test was utilized to analyze differences of Risser stage across genders and the three groups. The comparisons between males and females overall, and between the three age groups, were performed using one-way ANOVA followed by post hoc Bonferroni correction. The correlation of spinopelvic parameters was investigated using the Pearson correlation test. Association between PI and age, gender, Risser sign, and other radiographic parameters were assessed using Generalized Linear Modelling (GLM) analysis. A p-value of < 0.05 was considered statistically significant.

Results

In this study, we enrolled 217 participants, consisting of 112 males (51.6%) and 105 females (48.4%), aged between 4 and 15 years, with an average age of 12.19 years. The cohort was divided into three age groups: 21 participants were between 4 and 7 years, 60 participants between 8 and 11 years, and 136 participants between 12 and 15 years. The distribution of key spinal measurements—SS, PT, PI, LL, TK, T1 slope, C7 slope, cSVA, and C2–7 Cobb angle—was normally distributed across genders.

As described in Table 1, this study found the average pelvic incidence to be 39.3 ± 10.2°, showing no significant variance across the age groups (35.9 ± 8.2°, 38.4 ± 10.4°, and 40.1 ± 10.3°; p = 0.163) nor between genders (39.1 ± 9.9° for males and 39.5 ± 10.7° for females; p = 0.7324). Pelvic tilt was 7.3 ± 9.2°, demonstrating significant variances across age groups (5.9 ± 8.8° vs. 4.0 ± 8.2° vs. 8.9 ± 9.3°; p = 0.0018). This variance was more pronounced in female participants (5.2 ± 10.0° vs. 4.7 ± 8.8° vs. 10.7 ± 10.1°; p = 0.013). Further post hoc analyses revealed that, within the overall and female, the 12–15 years age group displayed significantly higher pelvic tilt compared to those in the 8–11 years age group. Significant gender differences were also observed (6.0 ± 7.7° for males vs. 8.6 ± 10.2° for females; p = 0.0341) (described in Table 4). The average sacral slope across all participants was 32.0 ± 8.6°, with no significant differences across age groups or between genders (p = 0.0608). The average lumbar lordosis was 46.5 ± 11.7°, showing no age group differences but notable gender differences (48.3 ± 10.6° for males vs. 44.9 ± 12.7° for females; p = 0.036), with males exhibiting higher LL (described in Table 4), which correlates with the larger SS in men and the associated SS-LL relationship. No significant LL differences were noted across the age groups (p = 0.0926).

Table 1 Distribution of parameters for the three age groups
Full size table

The average TK for all participants was 30.5 ± 10.5°, with significant gender differences observed (32.6 ± 10.5° for males vs. 28.6 ± 10.4° for females; p = 0.005) (described in Table 4), but no differences across age groups. The mean values for T1 slope, C7 slope, and C2–7 Cobb angle were 19.2 ± 8.8°, 16.4 ± 9.1°, and 13.4 ± 11.8°, respectively, with no statistical differences across age groups or genders. The cSVA, indicative of cervical spine sagittal balance, was observed to average 7.8 ± 20.5, revealing significant disparities across age groups (− 3.7 ± 15.7° vs. 2.7 ± 21.1° vs. 11.8 ± 19.9°; p < 0.001). Such variations were more pronounced in males (− 6.3 ± 16.6° vs. 1.8 ± 20.3° vs. 14.5 ± 20.4°; p = 0.0019). Subsequent post hoc analysis elucidated that, for both the overall and male cohorts, the 12–15 years age group exhibited notably higher values in comparison to both the 4–7 years and the 8–11 years groups.

Analysis presented in Table 2 reveals a statistically significant positive correlation between age and Risser sign, pelvic tilt (PT) and cervical sagittal vertical axis (cSVA), with coefficients of determination (R2) at 0.77, 0.16 and 0.25, respectively. The correlation between Risser sign and both PT and cSVA is evident, with coefficients of determination (R2) at 0.19 and 0.22, respectively. Furthermore, the relationship between pelvic incidence (PI) and PT, as well as sacral slope (SS) and lumbar lordosis (LL), aligns with patterns observed in adult populations, showing R2 values of 0.60, 0.52, and 0.33, respectively. Notably, PT exhibits a negative correlation with SS (R2 = 0.36), while SS is positively correlated with LL (R2 = 0.77). Additionally, a positive correlation exists between LL and thoracic kyphosis (TK) (R2 = 0.41), whereas LL and cSVA are negatively correlated (R2 = − 0.22). TK demonstrates a positive correlation with the cervical spine parameters T1 slope (T1S), C7 slope (C7S), and C2–7 Cobb angle, with R2 values of 0.61, 0.56, and 0.27, respectively. Both T1S and C7S show a positive correlation with cSVA and C2–7 Cobb angle, with R2 values of 0.83, 0.34, and 0.46, respectively. In a similar vein, C7S exhibits a positive correlation with cSVA and C2–7 Cobb angle (R2 = 0.24 and R2 = 0.46, respectively).

Table 2 Pearson correlation coefficient between different parameters
Full size table

Table 3 illustrates the distribution of Risser Sign stages within three distinct cohorts. Group A predominantly comprised individuals at Risser Sign stage 0, totaling 21, with an absence of participants in stages 1–5. In contrast, Group B encompassed 57 participants at stage 0 and 3 at stage 1, with no representation in higher stages. Group C, aged 12–15, includes all Risser sign stages, ranging from 19 participants at stage 0 to 14 at stage 5. It also included 8 participants at stage 1, 29 at stage 2, 21 at stage 3, and 45 participants at stage 4, illustrating a diverse Risser Sign stage distribution across this cohort. Significant variations were observed in the distribution of the Risser Sign across the three age cohorts, with a p-value of < 0.001.

Table 3 Distribution of stages of Risser sign in three groups
Full size table

Generalized Linear Modelling (GLM) analysis was performed to examine the relationships between PI and age, sex, stage of Risser sign and the other radiographic parameters. The analysis revealed that SS and PT were significantly correlated with PI, bearing coefficients of − 0.0004 and − 0.0005, respectively (both with p-values less than 0.001). Moreover, LL and TK also demonstrated significant associations with PI, with coefficients of − 0.0001 and 0.0001, respectively (Table 4). Interestingly, while age and gender did not significantly affect PI (p-values of 0.549 and 0.644, respectively), the Risser sign showed a subtle effect. Specifically, Risser 3 was significantly linked to an increase in PI (coefficient 0.0016, p = 0.04) compared to the baseline of Risser 0, suggesting developmental changes in pelvic morphology during this stage. T1 slope (T1S), C7 slope (C7S), and cervical spine vertical alignment (cSVA) were also assessed, with T1S displaying a modest but significant negative correlation with PI (coefficient − 0.000087, p = 0.026). In contrast, C7S and cSVA, along with the Cobb angle from C2 to C7 (C2–7 Cobb), did not exhibit statistically significant effects (Table 5).

Table 4 Results of sex-difference comparison for each parameter
Full size table
Table 5 Generalized linear modelling (GLM) analysis of PI and age, sex, stage of Risser sign, and other parameters
Full size table

Discussion

In pediatric surgery, attention has recently focused on the sagittal contour of the spine and the restoration of adequate thoracic kyphosis and lordosis. Yu et al. [8] confirmed these findings, showing a high incidence of cervical kyphosis in adolescent and young adult individuals.

Pelvic morphology has been reported to significantly influence the spine and whole sagittal balance [9]. More pain and disability with postoperative malalignment of cervical sagittal parameters [10]. Better understanding of normal spinopelvic balance in pediatric population could help spine surgeons comprehensively evaluate patients and prepare the appropriate treatment strategies for each case. However, spinopelvic sequences in children have been rarely reported in recent years. The major goals of this study were to report sagittal plane spinopelvic parameters of a group of health pediatric population. To the best of our knowledge, this is the first large-sample study in the literature that uses the standard standing EOS examination to examine the sagittal alignment of children from the cervical spine to the pelvis and provides a detailed analysis of the correlation between the pelvis, lumbar spine, thoracic spine, and cervical spine regions.

Spinopelvic parameters in our cohort were comparable to previous reported data in the pediatric population [11], moreover our results demonstrate the large variability of cervical angles among children spine [12]. Interestingly, in this study, Risser 3 was significantly linked to an increase in PI, this finding suggests that during Risser stage 3, there are consequential changes in the relationship between the pelvis and the spine, which in turn affect the measurements of pelvic incidence angles. This information could be crucial for a deeper understanding of the changes occurring in the skeletal structures of children and adolescents during different growth stages. However, these results require further validation through studies involving larger datasets.

The incidence of adolescent idiopathic scoliosis is significantly higher in females than in males [6], so we analyzed the effect of gender on sagittal sequences in asymptomatic Chinese children. We found significant sexual differences in the three parameters, which are PT, LL, and TK. Notably, females exhibited a greater PT, suggesting a more pronounced posterior pelvic tilt in girls, which logically accounts for the smaller SS observed (p = 0.0950). Compared to females, males demonstrated significantly higher values of LL and TK, with a notable positive correlation between LL and TK. These findings are in alignment with the research conducted by Mac-Thiong and colleagues [13], emphasizing the impact of pelvic positioning on spinal alignment. The influence of sex on PT might be associated with the differential development of pelvic morphology between males and females [14]. Furthermore, our results highlighted significant differences between the age groups of 8–11 and 12–15 years (p = 0.0003), with PT exhibiting significant variation across all age groups (p = 0.0018), indicating notable changes in PT with age, particularly among females (p = 0.013).

Another parameter exhibiting age-related variation is cSVA, for which significant differences were observed across the three age groups (p < 0.001). Contrary to PT, the variation in cSVA was more pronounced among males (p = 0.0019). Notable distinctions in cSVA were found between three groups, the group C exhibited notably higher values in comparison to both Group B and C, indicating that changes in the sagittal alignment of the cervical spine.

The cervical spine, a highly mobile segment, plays an important role in maintaining horizontal gaze. The impact of cervical spine sagittal plane deformity on the coronal plane of the spine in patients with adolescent idiopathic scoliosis [15], and scoliosis correction has a great impact on the cervical spine sagittal plane balance [16]. Therefore, understanding the normal physiological cervical sagittal sequence in children will provide a deeper understanding of the treatment and evaluation of AIS. C2–7Cobb is the most used measurement method to reflect cervical lordosis, but not all normal people’s cervical spines are lordotic [17]. We measure C2–7Cobb in children to show that in children. T1S [18] is a morphological parameter that describes the position of the thorax and is also a junctional parameter connecting the cervical and thoracic spine. The relationship between T1S and C2–7Cobb is like the relationship between SS and lumbar lordosis [19]. Lee et al. [20] found comparable values in an Asiatic asymptomatic population of children with a mean C2–7Cobb angle of − 4.8 ± 12°. Our data conflict with this result. Oe et al. [21] suggested that T1 slope increased the C2–C7 lordotic angle, and the increased C2–C7 lordosis may keep the C2–C7 sagittal vertical axis decreased by a continuous and compensatory principle. However, due to reasons such as sternum obstruction of the T1 vertebral body, some scholars proposed C7S as a supplementary parameter. C7 slope also is important for overall sagittal alignment, as it acts as a link between the occipitocervical and thoracolumbar spine and may anticipate the future of the spinal sagittal alignment after fusion surgeries [22, 23].

Pelvic incidence is correlated not only with spinopelvic parameters such as PT, SS, LL, and cSVA but also shows a significant association with Risser sign, reflecting the bone maturity [24,25,26]. However, this study is confined to establishing correlations based on radiographic outcomes. The effects of gender and bone maturity on the physiological mechanisms within the pelvic and spine, and the compensatory functions of these regions, necessitates more in-depth investigation.

However, this study is not without limitations. First, the precise identification of anatomical landmarks in young children is challenging due to the incomplete ossification of bones, especially in areas such as the femoral head. Despite these challenges, the inter- and intra-observer reliability remained within an acceptable range. The retrospective design and selection bias inherent in the outpatient screening process may affect the generalizability of our findings. Future research should consider longitudinal designs and a broader demographic to elucidate the developmental trajectories of spinopelvic alignment in adolescents and their impact on spinal alignment. This research establishes normative reference values for spinopelvic sagittal parameters in asymptomatic Chinese children. However, its clinical application remains unexplored. Another limitation is that it was a single-center study. To enhance future investigations, the research consortium is establishing a multi-institutional data exchange platform to encompass a broader cohort.

Conclusion

Significant variations in PT and cSVA across diverse age cohorts were identified, highlighting notable disparities in the distribution of PT and cSVA values within the Chinese pediatric population. Additionally, discernible gender-based differences in PT, LL, and TK were observed. The observed correlation in spinopelvic parameter could enhances our understanding of compensatory mechanisms within spinal regions.