Secondary Logo

Journal Logo

YOUNG INVESTIGATOR AWARD

2020 Young Investigator Award Winner: Age- and Sex-related Normative Value of Whole-body Sagittal Alignment Based on 584 Asymptomatic Chinese Adult Population From Age 20 to 89

Hu, Zongshan PhD∗,¶; Man, Gene Chi Wai PhD∗,¶; Yeung, Kwong Hang MSc†,¶; Cheung, Wing Hoi PhD∗,§,¶; Chu, Winnie Chiu Wing MD†,¶; Law, Sheung Wai MD∗,§; Lam, Tsz Ping MD∗,§,¶; Zhu, Zezhang MD‡,¶; Qiu, Yong MD‡,¶; Cheng, Jack Chun Yiu MD∗,§,¶

Author Information
doi: 10.1097/BRS.0000000000003187
  • Free

The prevalence of adult spinal deformity (ASD) has been reported to be as high as 60% in the elderly population.1 Surgical treatment of ASD patients has been increasingly performed for patients with deformity progression, neural compromise, as well as pain and functional disabilities which are not responsive to conservative treatment.2,3 For patients requiring surgical treatment with implants and spinal fusion, restoration of “a more normal sagittal balance” is a key goal for ASD surgery.4 Most reports on normative values of sagittal alignment in asymptomatic subjects are primarily based on the spinal alignment data.5 There is growing recognition of the importance of documenting the whole-body sagittal alignment, which in addition to the spinal alignment also take reference of co-existing lower limb compensatory mechanisms that might significantly affect the planning and outcome of treatment particularly for the elderly patients.

In spinal deformity, physiological efforts to maintain horizontal gaze and upright posture often necessitate the recruitment of compensatory mechanisms in the spinal column itself, and in the pelvis and lower limbs. The availability of low-radiation biplanar radiograph imaging system with 3D capability (EOS imaging system) has enabled more realistic real-time assessment of whole-body sagittal alignment from head to foot in standing position with significantly less distortion ÿrtifacts.6,7 Using this novel imaging technology, knee flexion, along with ankle flexion, pelvic retroversion/hip extension have been identified as additional compensation mechanisms that could be present in ASD patients.8

One of the key goals for surgical realignment of ASD is the optimization of personalized preoperative sagittal realignment planning taking reference to the normal age- and sex-matched values for the specific ethnic group.8 Previous studies have shown that populations with different ethnicity background could present with significant differences in the sagittal spinopelvic alignment.9–11 The normative values of whole-body sagittal alignment in Chinese adult population, however, have not been reported

To address the knowledge gap, the objective of this study was to establish age- and sex-related normative values of whole-body sagittal alignment in asymptomatic Chinese adult population aged 20 to 80 years, and to investigate the changes and possible associated compensation mechanisms across the different age groups.

SUBJECTS AND METHODS

Subjects

Asymptomatic Chinese volunteers were recruited community-wide from the whole of Hong Kong through designed advertisements, flyers and recruitment brochures. Subjects were all interviewed by trained medical staff following strict protocols with criteria for inclusion of age between 20 and 89 years with a validated Oswestry Disability index (ODI) scoring <20%. The exclusion criteria were: presence of low back pain or regular low back pain; previous spine, pelvis, or lower-limb pathology that could affect the spine; previous surgery on spine, pelvis, or lower limb; or pregnancy.5 Demographic characteristics of the subjects were recorded including age, body height, and body weight. Body mass index (BMI) was determined. The study was approved by our institutional review board (CREC Ref. No.: 2017.689) and all participants provided written informed consent.

Low-dose Biplanar Whole-body Radiographic Assessment

All subjects underwent whole body biplanar stereographs (EOS imaging, Paris, France) with a standardized radiographic protocol by a team of experienced radiographer.12,13 Subjects were instructed to stand in a comfortable position with hips and knees extended and with hands on a support.14 EOS images were measured using validated software (Surgimap, Nemaris Inc., New York, NY) for sagittal parameters (Figure 1).15 Spinal parameters included thoracic kyphosis (T5–12, TK) and lumbar lordosis (L1–S1, LL). Pelvic parameters included: pelvic incidence (PI), pelvic tilt (PT), sacral slope (SS). Global sagittal parameters were sagittal vertical axis (SVA) and T1 pelvic angle (TPA: the angle between the line from the femoral head axis to the centroid of T1 and the line from the femoral head axis to the middle of the S1 superior endplate). Lower limb parameters evaluated included knee flexion angle (KneeFlex: angle between the mechanical axis of the femur and the mechanical axis of the tibia) and ankle dorsiflexion angle (AA: angle between the mechanical axis of the tibia and the vertical).16 In clinical practice, the outline of thoracic vertebra above T5 on the x-ray radiographs are often difficult to identify and mark in the sagittal plane, owing to the obstruction of rib cage and upper arm. In the classical study on Lenke classification, T5-T12 kyphosis was used as TK to define Sagittal Thoracic Modifiers.17 Then a large number of studies adopted this landmark to measure TK, including our previous published articles; T5-T12 kyphosis was also used as a key parameter to evaluate clinical outcomes.11,18

Figure 1
Figure 1:
Illustration of measurements of spinal, pelvic, global and lower-limb parameters in sagittal radiograph, including TK, LL, TPA, PI, PT, KA, and AA.17 AA indicates ankle dorsiflexion angle; KA, KneeFlex angle; LL, lumbar lordosis; PI, pelvic incidence; PT, pelvic tilt; TK, thoracic kyphosis; TPA, T1-pelvis angle.

The subjects were subdivided for males versus females. In addition, they were further assigned into seven age groups: Group I, 20 to 29 years; Group II, 30 to 39 years; Group III, 40 to 49 years; Group IV, 50 to 59; Group V, 60 to 69; Group VI, 70 to 79; Group VII, 80 to 89 years for the analysis of the changes in whole-body and spinal sagittal alignment with increasing age.

All the parameters were measured by two independent observers (Z.H. and K.H.Y.). Intraobserver and interobserver variations were estimated by using intraclass correlation coefficient (ICC), which were graded using previously described semi-quantitative criteria: excellent (ICC ≥0.9), good (0.7≤ICC < 0.9), acceptable (0.6 < ICC≤0.7), poor (0.5≤ICC < 0.6), or unpredictable (ICC <0.5).19

Statistical Analysis

Data were expressed as mean ± standard deviation. The measurements were tabulated and analyzed using the SPSS version 19.0 software (SPSS Inc., Chicago, IL). Comparisons of means between variables were performed using an unpaired Student t test. Comparisons among age groups were made with analysis of variance, and the multiple comparisons were done. Correlations between variables were analyzed using the Pearson correlation coefficient. The level of significance was set at P < 0.05. The sample size calculation is based on Jennen-Steinmetz et al's20 approach using the probability content covered by the estimated reference interval. According this approach, to construct a 95% reference interval, the minimum sample size would be 482 for the parametric approach (confidence probability = 0.9, tolerance margin = 0.075). To ensure a reasonably distributed sample, we will need to recruit at least 40 males and 40 females for each age group. This sample size is similar to that of a previous study on the Japanese population.5

RESULTS

A total of 584 subjects were successfully recruited with the demographic data distribution and a minimum of 40 subjects of each sex in each age group as shown in Table 1. The average age of the subjects was 50.1 years (range, 20–89) and the BMI was 24.1 ± 6.8. The average ODI score was 6.7 ± 2.5 (range, 0–18), reflecting the asymptomatic cohort that matched with the inclusion criteria.

TABLE 1
TABLE 1:
Demographic Distribution of Study Participants

The intra- and interobserver ICCs for estimating the whole-body sagittal parameters were from 0.85 to 0.96, suggesting good to excellent reliability of these measurements among the two observers (Table 2). Mean values of spinal parameters were 26.6° ± 9.8° for TK and 42.4° ± 11.1° for LL. Mean values of pelvic parameters were 13.2° ± 9.1° for PT and 44.5° ± 11.4° for PI. The average values of global alignment were 20.7 ± 27.4 mm for SVA and 11.3° ± 8.4° for TPA. The mean values of lower-limb parameters, KA and AA were 2.8° ± 6.3° and 3.3° ± 3.5°, respectively.

TABLE 2
TABLE 2:
Intra- and Inter-rater Reliability Test for all Radiographic Parameters

The average values and overall trend for each sagittal variable in males and females by decade were shown in Table 3 and Figure 2. Across the different age groups, TK showed steady increasing trend while LL gradual decrease in both sexes (Table 3, Figure 2A, B). PT in males is greater than in females across all age groups with age-related gradual increase till age 60 years followed by accelerated increase afterwards (Table 3, Figure 2C, Figure 3A–C). PI remained relatively stable in both males and females (Table 3, Figure 2D, Figure 3). Global sagittal parameters, TPA and SVA, increased gradually with age (Table 3, Figure 2E and F). For the lower limb, significant differences were found between males and females from young age to 60s in terms of KA and AA, but the differences were less obvious after 60s. Both KA and AA slowly increased after 20s, and become more prominent after 50s (Table 3, Figure 2G and H, Figure 3).

TABLE 3
TABLE 3:
Mean Value of Whole-body Sagittal Parameters in Age Groups Between Males and Females
Figure 2
Figure 2:
Changes in spinal, pelvic, global, and lower-limb alignment parameters with age in males and females.
Figure 3
Figure 3:
Representative illustration of whole-body sagittal alignment from young adult to elder. Females at (A) 21 years, (B) 50 years, and (C) 82 years, respectively. From young adult to old-aged, thoracic kyphosis showed steady increase, whereas lumbar lordosis decreased. Pelvic tilt increased with age, and remarkable increase was observed from middle age to old age. Global sagittal parameters, T1 pelvic angle, and sagittal vertical axis were increased gradually with aging, wherein more pelvic and lower-limb alignments were recruited to maintain the global balance.

The whole-body sagittal alignment was found to vary with age and associated compensation mechanism from spine to lower limb (Table 4). Although the TPA and SVA were both significantly correlated with spinal, pelvic, and lower-limb alignment, a stronger tendency was observed in TPA as compared with SVA. In addition, there was correlation of TPA with other spinal, pelvic, and lower-limb parameters in younger (<50 years) and older adults (≥50 years) (Table 5). In comparison, the older adult group had a stronger correlation of TPA with PT and KA, whereas the younger adult group had stronger correlation with TK.

TABLE 4
TABLE 4:
Correlation Coefficient Between Radiographic Variables
TABLE 5
TABLE 5:
Correlation Coefficient Between TPA and Other Radiographic Variables in Younger and Older Groups

DISCUSSION

This study represents a prospective cross-sectional analysis of whole-body sagittal alignment incorporating the sagittal spinal, pelvic and lower-limb alignment with equal age and sex distribution, in a large cohort of asymptomatic subjects from age 20 to 89 years based on biplanar whole-body standing radiographs. Based on the findings, a comprehensive normative reference data for whole-body sagittal alignment was constructed for each sex and age group from 20 to 80 years in asymptomatic Chinese adult population.

Dubousset21 introduced the well-known theory “cone of economy,” which described the physiological mechanism in maintaining the head center of gravity over the pelvis to achieve an energy efficient mechanism for ambulation and upright posture. The body adapts to changes in this balance through regulating the center of gravity over as narrow a perimeter as possible. Various compensation mechanisms serve to maintain sagittal balance to achieve an energy efficient mechanism across the different age groups.

Remarkable variability in sagittal spinal alignment with increasing age has been reported in previous studies dedicated to optimizing and refining alignment target goals for surgical planning.22,23 Several authors have investigated age-related spinal alignment changes among asymptomatic volunteers. Gelb et al24 reported that increasing age in asymptomatic middle- and old-age volunteers is associated with a more anterior SVA with loss of lumbar lordosis. Yukawa et al5 conducted a large-scale study to establish standard values of sagittal spinal parameters in Japanese population. However, reports on normative values of age-related whole-body sagittal alignment from spine to lower limb were lacking. In the present study, we have shown steady increase of TK with associated decrease in LL with advancing age. Global sagittal parameters, TPA and SVA, were increased gradually with aging with a sudden increase in KA and AA after 50s, signifying the recruitment of additional physiological compensatory mechanism in the lower limb in maintaining the sagittal global balance. In the classical study on Lenke classification, T5-T12 kyphosis was used as TK to define Sagittal Thoracic Modifiers.17 Then a large number of studies adopted this landmark to measure TK, including our previous published articles; T5-T12 kyphosis was also used as a key parameter to evaluate clinical outcomes.11,18

In our study, increasing age was correlated with decreased LL and increased TK, PT, KA, and AA (Table 4), which was in accordance with reported series. These age-related decreases in LL could have triggered the recruitment of compensation mechanism in the lower limb with resultant increase in PT and KA,25 an important observation for surgeons to take into consideration in the preoperative planning for ASD corrections particularly on the elderly patients.

Contradicting observations on sex-related differences among parameters of sagittal spinal and spinopelvic alignment have been reported. Studies5,9 showed that female subjects had higher values of LL and PI, whereas no differences in PI, SS, and PT were reported by other studies.10 The present study based on a much larger cohort confirmed the existence of a large sex difference in pelvic morphology with PT and PI varying across the different age groups. Interestingly, previous study showed that female groups with age >40 years had higher PI than that of 20 s and 30 s.5 They speculated that the birth experience is one of the reasons of higher PI in females aged >40 years. However, we did not observe similar results, which may be because of the difference in ethnicity and socioeconomic status. In the previous study from our joint research center, Zhu et al11 conducted an age-matched comparative study and found that reported that Chinese population subjects from Chinese populations had significantly smaller PI and SS than those from white populations. This suggested that Chinese and European population had a different pelvic morphology and orientation, which are strong determinants of the sagittal spinal alignment in the upright position.

The increasing availability of EOS whole-body standing radiographs has made possible newer studies on physiological postural compensatory mechanism across different age groups in recent years,26,27 especially on the recruitment of lower-limb compensation to counteract sagittal spinal deformity and loss of upright posture in the elderly.28 Jalai et al8 reported that KA proved a useful metric to quantify resulting compensation needed, and significantly correlated in all age groups with increasing offset in SVA and TPA. In this study, we further found that lower-limb parameters KA and AA showed remarkable increase after age 50 years (Figure 2G, H), which may indicate the activation of compensation mechanism of the lower limbs. Therefore, we use the age of 50 years as a cut-off to divide the cohort into young and older group for subgroup correlation analysis. The result showed that the age of 50 as a cut-off, the younger group below age of 50 had stronger correlation of TPA with TK whereas the older group had a stronger correlation with PT and KA (Table 5), thus supporting the observation that spinal adaptation might no longer be adequate in those with age of more than 50 s and that additional pelvic and lower- limb compensation mechanism need to be recruited for maintaining the global sagittal balance.29

Although it could have been useful to incorporate cervical sagittal parameters in the sagittal measures, we have followed the Schwab classification and SRS radiographic definition of Adult Spinal Deformity (defined by at least one of the following: coronal Cobb angle at least 20°, SVA at least 5 cm, PT at least 25°, and/or TK at least 60°) using the indicative key sagittal parameters from thoracic spine to lower limb.29,30 The compensation mechanism mainly contained PT, SVA, knee flexion, and so on, where there is no C2 vertical axis.8,31 As the cervical alignment is quite flexible, reports have shown that the measurement can be severely affected by the head position.32,33 Thus, currently, there is a lack of clear definition of the normative value and standardization of the cervical alignment assessment.

There were several limitations in this cross-sectional study. First, a larger-scale cross-sectional and longitudinal studies could help to provide more further details. Additionally, as this study was based only on the Chinese population, similar studies in different ethnic groups would certainly help to provide additional specific reference data.34 Presently, China has a population of >1.3 billion people and a total of 56 different ethnic groups are recognized in this country, of which the Han Chinese group has the greatest population with 1.2 billion members.35,36 In this study, the Chinese subjects were recruited. Therefore, the generalizability may be a limitation of this study. In addition, T1, T4, and T5 were all used as the upper end vertebra of TK, whereas T5 is the most clinically useful.1,5 In clinical practice, the outline of thoracic vertebra above T5 on the x-ray radiographs is often difficult to identify and mark in the sagittal plane, because of the obstruction of rib cage and upper arm.

CONCLUSION

This study presented a comprehensive study of whole-body sagittal alignment based on a large cohort of asymptomatic population, which could serve as an age- and sex-specific reference value for spine surgeons when assessing and planning for potential correction surgery. Age can influence the recruitment of compensation mechanism that involves more pelvic and lower-limb mechanisms for elderly people.

Key Points

  • This study presented a comprehensive study of whole-body sagittal alignment based on a large cohort of asymptomatic Chinese population.
  • Age- and sex-specific sagittal alignment database could provide reference value for spine surgeons when assessing and planning for potential correction surgery.
  • Age can influence the different pattern of compensation mechanism that involves more pelvic and lower limb mechanisms for elderly people.

Acknowledgments

The authors are deeply grateful to have Dr. Huanxiong Chen, Dr. Ka-Yee Cheuk, Ms. Wing-yin Vivian Hung, Ms. Wai-Ping Fiona Yu, Ms. Ka-lo Cheng, Ms. Ka-Ling Echo Tsang, and Ms. Wing-Lam Josephine Yau, for their contribution in subject recruitment and data collection.

References

1. Schwab F, Dubey A, Gamez L, et al. Adult scoliosis: prevalence, SF-36, and nutritional parameters in an elderly volunteer population. Spine (Phila Pa 1976) 2005; 30:1082–1085.
2. Glassman SD, Schwab FJ, Bridwell KH, et al. The selection of operative versus nonoperative treatment in patients with adult scoliosis. Spine (Phila Pa 1976) 2007; 32:93–97.
3. Fu K-MG, Bess S, Shaffrey CI, et al. Patients with adult spinal deformity treated operatively report greater baseline pain and disability than patients treated nonoperatively; however, deformities differ between age groups. Spine (Phila Pa 1976) 2014; 39:1401–1407.
4. Glassman SD, Berven S, Bridwell K, et al. Correlation of radiographic parameters and clinical symptoms in adult scoliosis. Spine (Phila Pa 1976) 2005; 30:682–688.
5. Yukawa Y, Kato F, Suda K, et al. Normative data for parameters of sagittal spinal alignment in healthy subjects: an analysis of gender specific differences and changes with aging in 626 asymptomatic individuals. Eur Spine J 2018; 27:426–432.
6. Dubousset J, Charpak G, Dorion I, et al. A new 2D and 3D imaging approach to musculoskeletal physiology and pathology with low-dose radiation and the standing position: the EOS system. Bull Acad Natl Med 2005; 189:287–297. discussion 297–300.
7. Deschênes S, Charron G, Beaudoin G, et al. Diagnostic imaging of spinal deformities: reducing patients radiation dose with a new slot-scanning X-ray imager. Spine (Phila Pa 1976) 2010; 35:989–994.
8. Jalai CM, Cruz DL, Diebo BG, et al. Full-body analysis of age-adjusted alignment in adult spinal deformity patients and lower-limb compensation. Spine (Phila Pa 1976) 2017; 42:653–661.
9. Vialle R, Levassor N, Rillardon L, et al. Radiographic analysis of the sagittal alignment and balance of the spine in asymptomatic subjects. JBJS 2005; 87:260–267.
10. Mac-Thiong J-M, Roussouly P, Berthonnaud E, et al. Age-and sex-related variations in sagittal sacropelvic morphology and balance in asymptomatic adults. Eur Spine J 2011; 20:572.
11. Zhu Z, Xu L, Zhu F, et al. Sagittal alignment of spine and pelvis in asymptomatic adults: norms in Chinese populations. Spine (Phila Pa 1976) 2014; 39:E1–E6.
12. Dubousset J, Charpak G, Skalli W, et al. EOS: a new imaging system with low dose radiation in standing position for spine and bone & joint disorders. J Musculoskelet Res 2010; 13:1–12.
13. Fairbank J, Couper J, Davies J, et al. The Oswestry low back pain disability questionnaire. Physiotherapy 1980; 66:271–273.
14. Fechtenbaum J, Etcheto A, Kolta S, et al. Sagittal balance of the spine in patients with osteoporotic vertebral fractures. XXXXX 2016; 27:559–567.
15. Lafage R, Ferrero E, Henry JK, et al. Validation of a new computer-assisted tool to measure spino-pelvic parameters. The Spine Journal 2015; 15:2493–2502.
16. Diebo BG, Oren JH, Challier V, et al. Global sagittal axis: a step toward full-body assessment of sagittal plane deformity in the human body. Journal of Neurosurgery: Spine 2016; 25:494–499.
17. Lenke LG, Betz RR, Harms J, et al. Adolescent idiopathic scoliosis: a new classification to determine extent of spinal arthrodesis. JBJS 2001; 83:1169–1181.
18. Liu Z, Hu Zs, Qiu Y, et al. Role of clavicle chest cage angle difference in predicting postoperative shoulder balance in Lenke 5C adolescent idiopathic scoliosis patients after selective posterior fusion. Orthopaedic surgery 2017; 9:86–90.
19. Landis JR, Koch GG. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 1977; 33:363–374.
20. Jennen-Steinmetz C, Wellek S. A new approach to sample size calculation for reference interval studies. Stat Med 2005; 24:3199–3212.
21. Weinstein Raven Press, Dubousset J. Three-dimensional Analysis of the Scoliotic Deformity. The pediatric spine: principles and practice. 1994.
22. Lafage R, Schwab F, Challier V, et al. Defining spino-pelvic alignment thresholds: should operative goals in adult spinal deformity surgery account for age? Spine (Phila Pa 1976) 2016; 41:62–68.
23. Schwab FJ, Patel A, Shaffrey CI, et al. Sagittal realignment failures following pedicle subtraction osteotomy surgery: are we doing enough?: clinical article. J Neurosurg Spine 2012; 16:539–546.
24. Gelb DE, Lenke LG, Bridwell KH, et al. An analysis of sagittal spinal alignment in 100 asymptomatic middle and older aged volunteers. Spine (Phila Pa 1976) 1995; 20:1351–1358.
25. Iyer S, Lenke LG, Nemani VM, et al. Variations in sagittal alignment parameters based on age: a prospective study of asymptomatic volunteers using full-body radiographs. Spine (Phila Pa 1976) 2016; 41:1826–1836.
26. Cédric B, Pierre R, Jean-Charles LH, et al. Compensatory mechanisms contributing to keep the sagittal balance of the spine. Eur Spine J 2013; 22:S834–S841.
27. Diebo BG, Ferrero E, Lafage R, et al. Recruitment of compensatory mechanisms in sagittal spinal malalignment is age and regional deformity dependent: a full-standing axis analysis of key radiographical parameters. Spine (Phila Pa 1976) 2015; 40:642–649.
28. Ferrero E, Liabaud B, Challier V, et al. Role of pelvic translation and lower-extremity compensation to maintain gravity line position in spinal deformity. J Neurosurg Spine 2015; 24:436–446.
29. Schwab F, Ungar B, Blondel B, et al. Scoliosis Research Society—Schwab adult spinal deformity classification: a validation study. Spine (Phila Pa 1976) 2012; 37:1077–1082.
30. Schwab F, Patel A, Ungar B, et al. Adult spinal deformity—postoperative standing imbalance: how much can you tolerate? An overview of key parameters in assessing alignment and planning corrective surgery. Spine (Phila Pa 1976) 2010; 35:2224–2231.
31. Lafage V, Schwab F, Patel A, et al. Pelvic tilt and truncal inclination: two key radiographic parameters in the setting of adults with spinal deformity. Spine (Phila Pa 1976) 2009; 34:E599–E606.
32. Hansraj KK. Assessment of stresses in the cervical spine caused by posture and position of the head. Surg Technol Int 2014; 25:277–279.
33. Amabile C, Pillet H, Lafage V, et al. A new quasi-invariant parameter characterizing the postural alignment of young asymptomatic adults. Eur Spine J 2016; 25:3666–3674.
34. Zezhang Z, Leilei X, Feng Z, et al. Sagittal alignment of spine and pelvis in asymptomatic adults: norms in Chinese populations. Spine (Phila Pa 1976) 2014; 39:1–6.
35. Statistics CNBo. Statistical Bulletin of National Economic and Social Development in 2018. 2019.
36. Zhang H-G, Chen Y-F, Ding M, et al. Dermatoglyphics from all Chinese ethnic groups reveal geographic patterning. PLoS One 2010; 5:e8783.
Keywords:

adult spinal deformity; normative value; sagittal alignment; whole-body sagittal alignment

Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.