Eur Spine J DOI 10.1007/s00586-014-3563-9

ORIGINAL ARTICLE

Are there gender differences in sagittal spinal pelvic inclination before and after the adolescent pubertal growth spurt? Weijun Wang • Zhiwei Wang • Zhen Liu • Zezhang Zhu • Feng Zhu Xu Sun • Tsz Ping Lam • Jack Chun-yiu Cheng • Yong Qiu



Received: 10 October 2013 / Revised: 2 September 2014 / Accepted: 4 September 2014 Ó Springer-Verlag Berlin Heidelberg 2014

Abstract Purpose Significant progression of spinal deformity could occur during the peak of pubertal growth in adolescent idiopathic scoliosis (AIS). Gender differences in spinal and vertebral inclination have been reported in asymptomatic young adults and are thought to affect the risk of curve progression in male and female AIS. The present study aimed to investigate whether there were gender differences in the sagittal spinal-pelvic profile and whether any differences occurred before or developed during the normal pubertal growth spurt. Methods The sagittal up-right standing spine X-ray films from 71 male and 82 female asymptomatic adolescents were collected. The inclination of the global spine was analyzed by measuring the spino-sacral angle (SSA) and the spinal tilt (ST). Additionally, the inclination of the vertebrae (T1–L5), thoracic kyphosis (T4–T12) and lumbar lordosis were measured. These subjects were divided into the ascending phase (non-fused triradiate cartilage) G1 subgroup, the peak (fused triradiate cartilage and Risser grade 0–1) G2 subgroup and the late phase (Risser grade 2–5) of pubertal growth G3 subgroup. The comparisons between the males and females were carried out within the subgroups.

W. Wang  Z. Wang  Z. Liu  Z. Zhu  F. Zhu  X. Sun  Y. Qiu (&) Spine Surgery, The Affiliated Drum Tower Hospital of Nanjing University Medical School, Zhongshan Road 321, Nanjing 210008, China e-mail: [email protected] T. P. Lam  J. C. Cheng Department of Orthopaedics and Traumatology, The Chinese University of Hong Kong, Hong Kong, China

Results In the subgroups G1 and G2, the females showed a trend of less ventral inclination in the upper thoracic vertebrae (T1–T5) and greater dorsal inclination in the lower thoracic vertebrae (T7–T12), although the differences were not statistically significant. In the G3 subgroup, the females showed significantly larger SSA (133.7° ± 4.5° vs. 128.4° ± 4.0°), ST (96.3° ± 2.6° vs. 94.8° ± 3.4°) and dorsal inclination of T1 and T12–L2 than did the males (p \ 0.05). Conclusions Although a trend toward a more backward inclination of the spine and individual vertebrae might preexist during the ascending phase or peak of pubertal growth, the differences become more significant during the late stage of puberty. The observation could be related to relatively active anterior vertebral overgrowth that occurs in females during pubertal growth. Keywords Vertebral inclination  Gender differences  Puberty  Spinal alignment  Idiopathic scoliosis

Introduction Adolescent idiopathic scoliosis (AIS) is a three-dimensional torsional deformity of the spine manifested as lateral curvature on conventional radiographs; AIS occurs during pubertal growth, and the etiopathogenesis is unknown [1, 2]. Several scoliosis screening projects from different countries and regions have revealed a higher prevalence of AIS in females than in males [1, 3–9]. An increased female-to-male ratio was observed in patients with a larger Cobb angle. For patients with major curvature greater than 308, the ratio could be as high or higher than 10–1 [1, 3–9]. The underlying pathomechanisms for these gender differences in AIS have not been adequately studied. Despite

123

Eur Spine J

being the most common type of human spinal deformity, idiopathic scoliosis has not been identified in other vertebrates. It is hypothesized that the fully erect bipedal posture in human ambulation is associated with more dorsally inclined vertebrae relative to all other vertebrates because of gravity and muscle activity. It has been proposed that dorsally directed forces in humans might be involved in the development and progression of AIS curve in AIS in susceptible adolescents [10, 11]. A comparison of the sagittal spino-pelvic alignment between asymptomatic young adult males and females by Janssen et al. [12] showed that females had more dorsally inclined individual vertebrae in certain regions and along the entire spine than did males. The authors hypothesize that these differences might contribute to the higher incidence of progressive idiopathic scoliosis in females. Whether the gender difference in spinal and vertebral inclination is a pre-existing phenotype or a development during the peri-pubertal period in which significant curve progression of AIS could occur has not been clearly documented. This study aimed to compare the sagittal spinal profiles between normal males and females before and after the pubertal growth spurt.

Materials and methods Subjects A cross-sectional study was conducted to recruit healthy males and females 10–18 years of age from local primary and middle schools. The subjects underwent a forward bending test and scoliometer measurement of the trunk rotation angle by an experienced orthopedic surgeon (Y Qiu). The exclusion criteria were as follows: (1) clinically observed deformity in the spine, pelvis or lower limbs; (2) disease or deformity affecting the spine, pelvis or lower limbs; (3) history of back, hip or lower limb pain; (4) scoliometer reading of more than 5° [13]. Informed consent was obtained from the subjects and their parents. The study was approved by the clinical research ethics committee of the hospital.

Fig. 1 Illustration of the radiographic parameters of spinal sagittal alignment analysis

would be noted if there were discrepancies between the two sides of the iliac apophyses. The subjects with a Cobb angle of over 10° were excluded [14]. To understand whether the differences in spinal sagittal alignment were present before or developed during the pubertal growth spurt, the subjects were divided into three subgroups according to the Risser grade and the fusion status of the triradiate cartilage, as follows: non-fused triradiate cartilage (G1), fused triradiate cartilage with Risser grade 0–1 (G2) and a Risser grade of 2–5 (G3) [15]. Sagittal alignment analysis

X-ray films and subject subgrouping Standing full length postero-anterior and lateral digital radiographs of the spine were taken with a standard protocol. For the lateral radiographs, the subjects stood upright with elbows bent and upper arms forward-flexed at 45° (Fig. 1) [12]. The postero-anterior X-ray films were reviewed by a senior spine surgeon to determine the Risser grades, fusion status of triradiate cartilage and Cobb angle of the spine in the coronal plane. A higher Risser grade

123

The parameters describing the sagittal profile of the spine and pelvis were quantified on lateral X-ray films using Surgimap Spine (Nemaris, Inc.) (Fig. 1). The thoracic kyphosis angle (TK, T4–T12) and lumbar lordosis angle (LL, L1–S1) were measured. The inclination of the individual vertebra within the region of focus was determined by the angle between the tangent lines drawn along the superior endplate of the vertebrae and a horizontal line. The spinosacral angle (SSA) and the spinal tilt (ST) [16] were

Eur Spine J Table 1 Summary of gender and maturity of adolescents Male

Female

Risser grade: Sample size:

0 14

1 22

2 6

3 8

4 14

5 7

0 15

1 22

2 5

3 5

4 27

Subgroups

G1

G2

G3

G1

G2

Sample size

15

21

35

16

21

45

Age (years) Risser grade

10.7 ± 0.8 0.1 ± 0.4

12.4 ± 0.8 1.0 ± 0.2

15.1 ± 1.8 3.6 ± 1.0

10.6 ± 0.5 0.2 ± 0.4

12.0 ± 1.2 0.9 ± 0.3

14.8 ± 2 3.8 ± 0.8

5 8

G3

Subgroups: G1 subjects with non-fused triradiate cartilage, G2 subjects with fused triradiate cartilage and Risser grade 0–1, G3 subjects with fused triradiate cartilage and Risser grade 2–5 Table 2 The sagittal spinal profiles between male and female adolescents Gender

N

G1

G2

G3

Males

Females

Males

Females

Males

Females

15

16

21

21

35

45

TK (T4–T12) (°)

24.6 ± 10.3

22.2 ± 6.2

22.0 ± 9.6

21.7 ± 9.5

20.0 ± 7.6

22.3 ± 7.1

LL (L1–S1) (°)

47.1 ± 9.4

50.6 ± 11.0

47.6 ± 9.3

47.5 ± 14.5

44.9 ± 9.2

48.3 ± 9.9

SSA (°)

129.0 ± 7.6

133.9 ± 8.0

129.7 ± 7.0

132.4 ± 10.2

128.4 ± 4.0

133.7 ± 4.5*

ST (°)

96.9 ± 3.1

96.7 ± 4.2

95.2 ± 3.6

96.4 ± 6.9

94.8 ± 3.4

96.3 ± 2.6*

Comparisons between males and females within each of the subgroups were performed using Student’s t test Subgroups: G1 subjects with non-fused triradiate cartilage, G2 subjects with fused triradiate cartilage and Risser grade 0–1, G3 subjects with fused triradiate cartilage and Risser grade 2–5 * p \ 0.05

measured to present the global sagittal balance of the spine. Forward/ventral inclination was defined as a positive value, and backward/dorsal inclination as a negative value (Fig. 1). Two authors (WJ Wang and ZW Wang) independently and blindly performed the measurements to compare the inter-observer reliability. These measurements were repeated by the first author (WJ Wang) 4 weeks later to compare the intra-observer reliability. Statistical analysis The data analysis was performed using the Statistical Package for the Social Sciences. (Version 12.0, SPSS, Inc., Chicago, IL, USA). The intra- and inter-observer reliabilities of the parameters were analyzed using intraclass correlations. Comparisons of the chronological age and the radiographic parameters between the female and male subjects within each of the subgroups were performed using Student’s t test. The level of significance was defined as p B 0.05.

Results A total of 160 subjects were recruited for radiography examination. Seven subjects were excluded because of the

presence of scoliosis, abnormal development of vertebrae or Scheuermann’s disease. The radiographs of 82 females and 71 males were available for the final analysis. The number and the mean age of the subjects, as well as the gender distribution and Risser grades, are summarized in Table 1. There were two male and three female subjects with Risser grade 1 with non-fused triradiate cartilage and one male and two female subjects with Risser grade 0 with fused triradiate cartilage. The reliability analysis showed excellent intra- and inter-observer agreement in the parameters, with an intraclass correlation (ICC) greater than 0.9. The comparisons of the sagittal spinal pelvic profiles were carried out between the males and females within each of the three subgroups, and the results are shown in Table 2. No gender differences were identified in the TK and LL in the subgroups. In the subjects with non-fused triradiate cartilage or fused triradiate cartilage with Risser grade 0–1, no difference in SSA and ST was observed between the females and males. In the Risser grade 2–5 subgroup, the females had significantly larger SSA and ST values than the males (SSA: 133.7° ± 4.5° vs. 128.4° ± 4.0°; ST: 96.3° ± 2.6° vs. 94.8° ± 3.4°; p \ 0.05) In all three subgroups, the females showed less ventral inclination in the upper thoracic vertebrae (T1–T5) and

123

Eur Spine J Fig. 2 The mean sagittal vertebral inclination between males (n = 15) and females (n = 16) with non-fused triradiate cartilage (G1). No significant differences were observed between genders

Fig. 3 The mean sagittal vertebral inclination between males (n = 21) and females (n = 21) with fused triradiate cartilage and Risser grade 0–1 (G2). No significant gender differences were observed

greater dorsal inclination in the lower thoracic vertebrae (T7–T12). In the G3 subjects with Risser grade of 2–5, the females showed significantly less ventral inclination at T1 and significantly more dorsal inclination in the thoracolumbar vertebrae (T12–L2) than did males (Figs. 2, 3, 4). The differences in the G1 and G2 subgroups were not statistically significant.

Discussion Multiple studies have been conducted to explain the clinical observation of female predominance in the incidence

123

and risk of curve progression in AIS [1–9]. Analyzing the sagittal spino-pelvic alignment in asymptotic adults (at ages ranging from 20 to 49 years), Janssen et al. [12] observed a more dorsally inclined spine in females than in males. Basing on mechanical principles that dorsal shear loads could lead to rotational instability in the mid- and lower thoracic vertebrae [17], Janssen et al. [12] suggested that these differences might lead to regional instability and contribute to the increased occurrence of curve progression in female AIS patients. The most significant curve progression of AIS occurred during the pubertal growth period, at which time the vertebral growth plate and spinal processes show accelerated growth [18]; we focused on

Eur Spine J Fig. 4 The mean sagittal vertebral inclination between males (n = 35) and females (n = 45) with Risser stage 2–5 (G3). Female showed significantly less ventral inclination at T1 and a larger vertebral inclination at T12–L2

whether gender differences exist in relative spinal inclination angles and, if so, whether they are present before or develop during the peri-pubertal growth spurt. The normal growth pattern in humans during the peripubertal period is marked by rapid peak growth followed by a gradual decline. After the initiation of puberty, the growth velocity accelerates and peaks before the initiation of the fusion of iliac apoptosis (Risser grade 1), followed by gradually descending growth velocity to zero at Risser grade 5 [15]. The growth status during puberty could be gauged by several skeletal parameters such as the Risser grades, fusion status of the triradiate cartilage, fusion status of the greater trochanter, elbow ossification status, skeletal age and digital skeletal age in the hand and wrist et al. [19– 21]. In studies, adolescents with open triradiate cartilage are regarded to be in the ascending phase of growth, and those with fused triradiate cartilage and Risser grade 0–1 are in the peak of growth; Risser grades 2–5 indicate the late stage of pubertal growth [19]. Based on this concept, the adolescents in this study were divided into three subgroups according to the Risser grade and the fusion status of triradiate cartilage. Our study revealed a significantly larger SSA and ST in females than in males in the Risser grade 2–5 subgroup, in contrast to the Risser grade 0–1 subgroup with or without fused triradiate cartilage, in which no significant gender differences were observed. By comparing the individual vertebral inclinations in 60 asymptomatic young males and females (age 21–49 years), Janssen et al. [12] found that females had a more dorsally inclined entire spine (T1–L5 sagittal spinal inclination) than males. Females had less ventral inclination in the upper thoracic vertebrae and greater dorsal inclination in the lower thoracic and upper lumbar vertebrae, and these

differences were significant at T1–T5, T11 and T12 [12]. This study found more dorsally inclined vertebrae at T12– L2 in subjects with a Risser grade 2–5, not in the other two subgroups. The results of Janssen et al. [12] and this study suggested that a more backwardly inclined global spine in females than in males might develop during the late pubertal stage of adolescents rather than in the pre-pubertal stage. Because the AIS is exclusive to humans, Castelein et al. [10] postulated that the vertical position of the trunk in humans plays a role in the onset of AIS. Kouwenhoven et al. [17] found that the backward inclination of vertebrae could result in a rotational instability of vertebrae, which could result in asymmetric spinal growth and cause spinal deformity. Our findings concurred with those of Janssen et al. [12] showed that the observed significant gender differences in thoracolumbar vertebral inclination might predispose to a differentiated rotational instability of the spine between males and females, especially in later puberty and adulthood. These differences might contribute to the [17] higher incidence of curve progression in female AIS patients during puberty [1, 3–9]. Stokes and Windisch [18] found that the spinal growth of patients with scoliosis (between 10 and 20 years of age) occurs almost exclusively by height increases in the vertebrae, not the discs. It could be hypothesized that the more backwardly inclined spine and vertebrae in females with a Risser grade 2–5 might be because of the relatively active anterior vertebral overgrowth that has been documented in female AIS relative to age- and gender-matched controls [22–27]. A further longitudinal follow up study is necessary to investigate the prognostic value of vertebral and spinal inclination in curve progression in AIS.

123

Eur Spine J

A comparison on the inclination of the entire spine and the individual vertebrae in male and female AIS patients would be more direct in understanding the role of spinal and individual vertebrae inclination on the different incidence of curve progression in males and females. The vertebrae in the scoliotic curve would be wedged and inclined on the coronal plane, and these changes would result in difficulties in identifying the vertebral endplates on the sagittal plane and might lead to bias in determining vertebral inclination. Normal subjects were recruited in this study because of these concerns. Additional limitations in this study should be addressed as well. The sagittal spinal-pelvic alignment was analyzed using standing upright lateral X-ray films that presented a 2D image of the spine using computer-assisted semi-automatic measurement [12, 28]. This finding would lead to radiological exposure to the adolescents. The EOS imaging device, which can reconstruct a 3D image of the spine through biplanar radiographs with significantly reduced radiation exposure, is not widely available. In this study, the growth status was determined cross-sectionally by skeletal maturity parameters. The combination of using Risser grades and the fusion status of triradiate cartilage in this study was found to be an acceptable indicator of the pubertal growth status [19].

Conclusion Gender differences with respect to the inclination of the spine and the individual vertebrae and spinopelvic alignment were investigated in normal adolescents. Although the females with non-fused triradiate cartilage, fused triradiate cartilage with a Risser grade 0–1 and Risser grade 2–5 have a more backwardly inclined spine and individual vertebrae than do the males, the trend was more significant in the late stage of puberty. The observation could be related to relatively active anterior vertebral overgrowth in females occurring during puberty growth, which might contribute to the different incidence of curve progression between male and female AIS patients. Acknowledgments This work was supported by National Natural Science Foundation of China (81101335), National Post-doctoral Foundation of China (2012M52101062), National Key Clinical Specialty Construction Project in Orthopaedics and Jiangsu Province’s Key Medical Talents Project (RC2011149). Conflict of interest

None.

References 1. Weinstein SL, Dolan LA, Cheng JC et al (2008) Adolescent idiopathic scoliosis. Lancet 371:1527–1537

123

2. Wang WJ, Yeung HY, Chu WC et al (2011) Top theories for the etiopathogenesis of adolescent idiopathic scoliosis. J Pediatr Orthop 31:S14–S27 3. Raggio CL (2006) Sexual dimorphism in adolescent idiopathic scoliosis. Orthop Clin North Am 37:555–558 4. Luk KD, Lee CF, Cheung KM et al (2010) Clinical effectiveness of school screening for adolescent idiopathic scoliosis: a large population-based retrospective cohort study. Spine (Phila Pa 1976) 35:1607–1614 5. Brooks HL, Azen SP, Gerberg E et al (1975) Scoliosis: A prospective epidemiological study. J Bone Joint Surg Am 57:968–972 6. Kane WJ, Moe JH (1970) A scoliosis-prevalence survey in Minnesota. Clin Orthop Relat Res 69:216–218 7. Ueno M, Takaso M, Nakazawa T et al (2011) A 5-year epidemiological study on the prevalence rate of idiopathic scoliosis in Tokyo: school screening of more than 250,000 children. J Orthop Sci 16:1–6 8. Richards BS, Herring JA, Johnston CE et al (1994) Treatment of adolescent idiopathic scoliosis using Texas Scottish Rite Hospital instrumentation. Spine (Phila Pa 1976) 19:1598–1605 9. Lenke LG, Bridwell KH, Baldus C et al (1992) Cotrel-Dubousset instrumentation for adolescent idiopathic scoliosis. J Bone Joint Surg Am 74:1056–1067 10. Castelein RM, van Dieen JH, Smit TH (2005) The role of dorsal shear forces in the pathogenesis of adolescent idiopathic scoliosis-a hypothesis. Med Hypotheses 65:501–508 11. Janssen MM, Kouwenhoven JW, Schlosser TP et al (2011) Analysis of preexistent vertebral rotation in the normal infantile, juvenile, and adolescent spine. Spine (Phila Pa 1976) 36:E486– E491 12. Janssen MM, Drevelle X, Humbert L et al (2009) Differences in male and female spino-pelvic alignment in asymptomatic young adults: a three-dimensional analysis using upright low-dose digital biplanar X-rays. Spine (Phila Pa 1976) 34:E826–E832 13. Wong HK, Hui JH, Rajan U et al (2005) Idiopathic scoliosis in Singapore school children: a prevalence study 15 years into the screening program. Spine (Phila Pa 1976) 30:1188–1196 14. Bitan FD, Veliskakis KP, Campbell BC (2005) Differences in the Risser grading systems in the United States and France. Clin Orthop Relat Res 436:190–195 15. Dimeglio A (2001) Growth in pediatric orthopaedics. J Pediatr Orthop 21:549–555 16. Barrey C, Jund J, Noseda O et al (2007) Sagittal balance of the pelvis-spine complex and lumbar degenerative diseases. A comparative study about 85 cases. Eur Spine J 16:1459–1467 17. Kouwenhoven JW, Smit TH, van der Veen AJ et al (2007) Effects of dorsal versus ventral shear loads on the rotational stability of the thoracic spine: a biomechanical porcine and human cadaveric study. Spine (Phila Pa 1976) 32:2545–2550 18. Stokes IA, Windisch L (2006) Vertebral height growth predominates over intervertebral disc height growth in adolescents with scoliosis. Spine (Phila Pa 1976) 31:1600–1604 19. Dimeglio AMD, Canavese F, Charles P (2011) Growth and adolescent idiopathic scoliosis: when and how much? J Pediatr Orthop 31:S28–S36 20. Wang WW, Xia CW, Zhu F et al (2009) Correlation of Risser sign, radiographs of hand and wrist with the histological grade of iliac crest apophysis in girls with adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 34:1849–1854 21. Wang SF, Qiu Y, Ma ZL et al (2007) Histologic, Risser sign, and digital skeletal age evaluation for residual spine growth potential in Chinese female idiopathic scoliosis. Spine (Phila Pa 1976) 32:1648–1654 22. Cheung CSK, Lee WTK, Tse YK et al (2003) Abnormal peripubertal anthropometric measurements and growth pattern in

Eur Spine J adolescent idiopathic scoliosis: a study of 598 patients. Spine (Phila Pa 1976) 28:2152–2157 23. Yim AP, Yeung HY, Hung VW et al (2012) Abnormal skeletal growth patterns in adolescent idiopathic scoliosis–a longitudinal study until skeletal maturity. Spine (Phila Pa 1976) 37:E1148– E1154 24. Funao H, Tsuji T, Hosogane N et al (2012) Comparative study of spinopelvic sagittal alignment between patients with and without degenerative spondylolisthesis. Eur Spine J 21:2181–2187 25. Porter RW (2001) The pathogenesis of idiopathic scoliosis: uncoupled neuro-osseous growth? Eur Spine J 10:473–481

26. Guo X, Chau WW, Chan YL et al (2003) Relative anterior spinal overgrowth in adolescent idiopathic scoliosis. Results of disproportionate endochondral-membranous bone growth. J Bone Joint Surg Br 85:1026–1031 27. Zhu F, Qiu Y, Yeung HY et al (2006) Histomorphometric study of the spinal growth plates in idiopathic scoliosis and congenital scoliosis. Pediatr Int 48:591–598 28. Vrtovec T, Janssen MM, Pernus F et al (2012) Analysis of pelvic incidence from 3-dimensional images of a normal population. Spine (Phila Pa 1976) 37:E479–E485

123

Are there gender differences in sagittal spinal pelvic inclination before and after the adolescent pubertal growth spurt?

Significant progression of spinal deformity could occur during the peak of pubertal growth in adolescent idiopathic scoliosis (AIS). Gender difference...
794KB Sizes 1 Downloads 4 Views