Skip to main content
Top
Published in: BMC Musculoskeletal Disorders 1/2014

Open Access 01-12-2014 | Research article

Accelerated endochondral growth in adolescents with idiopathic scoliosis: a preliminary histomorphometric study

Authors: Xin Zheng, Weijun Wang, Bangping Qian, Shoufeng Wang, Zezhang Zhu, Bin Wang, Xu Sun, Yitao Ding, Yong Qiu

Published in: BMC Musculoskeletal Disorders | Issue 1/2014

Login to get access

Abstract

Background

Abnormal longitudinal growth has been identified in the early pubertal stage of idiopathic scoliosis (IS) and is thought to contribute to the development of scoliosis. This phenotype may be caused by abnormal endochondral ossification, but histological evidence is lacking. The aim of this study was to investigate whether there is abnormal endochondral ossification in IS patients at early stage of puberty by histomorphometric analysis of their iliac cartilage.

Methods

Fifty-two patients with IS and 19 controls were recruited and grouped according to their Risser grade (Group A: Risser grade 0 with Oxford stage 2–3; Group B: Risser grade 2). Group A consisted of 20 IS patients (mean age: 12.3 years) and 9 controls (mean age: 12.0 years), while Group B included 32 IS patients (mean age: 13.8 years) and 10 controls (mean age: 13.7 years). Biopsies of the iliac cartilage were harvested intra-operatively and prepared using routine histological methods. Histomorphometric analysis was performed to quantify the thickness of the hypertrophic zone, the area and number of chondrocytes in the cell-nest, and the number of chondrocytes in the proliferative zone using Image-Pro Plus software.

Results

In Group A, a significantly thicker hypertrophic zone and larger cell-nest area and number of cells within the cell-nest, and in the proliferative zone, were found in iliac cartilages from IS patients compared with those of controls (all P < 0.05). In group B however, there were no significant differences in histomorphometric parameters between IS patients and the controls.

Conclusions

The differences in the histomorphometric results between IS patients and their controls for patients with Risser grade 0 and Oxford grades 2 & 3, but not in those with Risser grade 2, indicated a pattern of accelerated endochondral growth in IS at the early stage of puberty, but not at the late stage.

Trial registration

Current Controlled Trials: ChiCTR-CCC-13003988. Registered 17 December 2013. http://​www.​chictr.​org/​usercenter/​project/​edit.​aspx?​proj=​6233.
Appendix
Available only for authorised users
Literature
1.
go back to reference Goldberg CJ, Dowling FE, Fogarty EE: Adolescent idiopathic scoliosis: is rising growth rate the triggering factor in progression?. Eur Spine J. 1993, 2: 29-36. 10.1007/BF00301052.CrossRefPubMed Goldberg CJ, Dowling FE, Fogarty EE: Adolescent idiopathic scoliosis: is rising growth rate the triggering factor in progression?. Eur Spine J. 1993, 2: 29-36. 10.1007/BF00301052.CrossRefPubMed
2.
go back to reference Barrios C, Cortes S, Perez-Encinas C, Escriva MD, Benet I, Burgos J, Hevia E, Piza G, Domenech P: Anthropometry and body composition profile of girls with nonsurgically treated adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 2011, 36: 1470-1477. 10.1097/BRS.0b013e3181f55083.CrossRef Barrios C, Cortes S, Perez-Encinas C, Escriva MD, Benet I, Burgos J, Hevia E, Piza G, Domenech P: Anthropometry and body composition profile of girls with nonsurgically treated adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 2011, 36: 1470-1477. 10.1097/BRS.0b013e3181f55083.CrossRef
3.
go back to reference Buric M, Momcilovic B: Growth pattern and skeletal age in school girls with idiopathic scoliosis. Clin Orthop Relat Res. 1982, 170: 238-242.PubMed Buric M, Momcilovic B: Growth pattern and skeletal age in school girls with idiopathic scoliosis. Clin Orthop Relat Res. 1982, 170: 238-242.PubMed
4.
go back to reference Guo X, Chau WW, Chan YL, Cheng JC: Relative anterior spinal overgrowth in adolescent idiopathic scoliosis. Results of disproportionate endochondral-membranous bone growth. J Bone Joint Surg Br. 2003, 85: 1026-1031. 10.1302/0301-620X.85B7.14046.CrossRefPubMed Guo X, Chau WW, Chan YL, Cheng JC: Relative anterior spinal overgrowth in adolescent idiopathic scoliosis. Results of disproportionate endochondral-membranous bone growth. J Bone Joint Surg Br. 2003, 85: 1026-1031. 10.1302/0301-620X.85B7.14046.CrossRefPubMed
5.
go back to reference Hagglund G, Karlberg J, Willner S: Growth in girls with adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 1992, 17: 108-111. 10.1097/00007632-199201000-00016.CrossRef Hagglund G, Karlberg J, Willner S: Growth in girls with adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 1992, 17: 108-111. 10.1097/00007632-199201000-00016.CrossRef
6.
go back to reference Lao LF, Shen JX, Chen ZG, Wang YP, Wen XS, Qiu GX: Uncoupled neuro-osseous growth in adolescent idiopathic scoliosis? A preliminary study of 90 adolescents with whole-spine three-dimensional magnetic resonance imaging. Eur Spine J. 2011, 20: 1081-1086. 10.1007/s00586-010-1471-1.CrossRefPubMed Lao LF, Shen JX, Chen ZG, Wang YP, Wen XS, Qiu GX: Uncoupled neuro-osseous growth in adolescent idiopathic scoliosis? A preliminary study of 90 adolescents with whole-spine three-dimensional magnetic resonance imaging. Eur Spine J. 2011, 20: 1081-1086. 10.1007/s00586-010-1471-1.CrossRefPubMed
7.
go back to reference Mao SH, Jiang J, Sun X, Zhao Q, Qian BP, Liu Z, Shu H, Qiu Y: Timing of menarche in Chinese girls with and without adolescent idiopathic scoliosis: current results and review of the literature. Eur Spine J. 2010, 20: 260-265.CrossRefPubMedPubMedCentral Mao SH, Jiang J, Sun X, Zhao Q, Qian BP, Liu Z, Shu H, Qiu Y: Timing of menarche in Chinese girls with and without adolescent idiopathic scoliosis: current results and review of the literature. Eur Spine J. 2010, 20: 260-265.CrossRefPubMedPubMedCentral
8.
go back to reference Siu King Cheung C, Tak Keung Lee W, Kit Tse Y, Ping Tang S, Man Lee K, Guo X, Qin L, Chun Yiu Cheng J: Abnormal peri-pubertal anthropometric measurements and growth pattern in adolescent idiopathic scoliosis: a study of 598 patients. Spine (Phila Pa 1976). 2003, 28: 2152-2157. 10.1097/01.BRS.0000084265.15201.D5.CrossRef Siu King Cheung C, Tak Keung Lee W, Kit Tse Y, Ping Tang S, Man Lee K, Guo X, Qin L, Chun Yiu Cheng J: Abnormal peri-pubertal anthropometric measurements and growth pattern in adolescent idiopathic scoliosis: a study of 598 patients. Spine (Phila Pa 1976). 2003, 28: 2152-2157. 10.1097/01.BRS.0000084265.15201.D5.CrossRef
9.
go back to reference Wang WJ, Hung VW, Lam TP, Ng BK, Qin L, Lee KM, Qiu Y, Cheng JC, Yeung HY: The association of disproportionate skeletal growth and abnormal radius dimension ratio with curve severity in adolescent idiopathic scoliosis. Eur Spine J. 2010, 19: 726-731. 10.1007/s00586-009-1247-7.CrossRefPubMedPubMedCentral Wang WJ, Hung VW, Lam TP, Ng BK, Qin L, Lee KM, Qiu Y, Cheng JC, Yeung HY: The association of disproportionate skeletal growth and abnormal radius dimension ratio with curve severity in adolescent idiopathic scoliosis. Eur Spine J. 2010, 19: 726-731. 10.1007/s00586-009-1247-7.CrossRefPubMedPubMedCentral
10.
go back to reference Wang WJ, Yeung HY, Chu WC, Tang NL, Lee KM, Qiu Y, Burwell RG, Cheng JC: Top theories for the etiopathogenesis of adolescent idiopathic scoliosis. J Pediatr Orthop. 2011, 31: S14-S27.CrossRefPubMed Wang WJ, Yeung HY, Chu WC, Tang NL, Lee KM, Qiu Y, Burwell RG, Cheng JC: Top theories for the etiopathogenesis of adolescent idiopathic scoliosis. J Pediatr Orthop. 2011, 31: S14-S27.CrossRefPubMed
11.
go back to reference Zhu F, Qiu Y, Yeung HY, Lee KM, Cheng JC: Histomorphometric study of the spinal growth plates in idiopathic scoliosis and congenital scoliosis. Pediatr Int. 2006, 48: 591-598. 10.1111/j.1442-200X.2006.02277.x.CrossRefPubMed Zhu F, Qiu Y, Yeung HY, Lee KM, Cheng JC: Histomorphometric study of the spinal growth plates in idiopathic scoliosis and congenital scoliosis. Pediatr Int. 2006, 48: 591-598. 10.1111/j.1442-200X.2006.02277.x.CrossRefPubMed
12.
go back to reference Normelli H, Sevastik J, Ljung G, Aaro S, Jonsson-Soderstrom AM: Anthropometric data relating to normal and scoliotic Scandinavian girls. Spine (Phila Pa 1976). 1985, 10: 123-126. 10.1097/00007632-198503000-00002.CrossRef Normelli H, Sevastik J, Ljung G, Aaro S, Jonsson-Soderstrom AM: Anthropometric data relating to normal and scoliotic Scandinavian girls. Spine (Phila Pa 1976). 1985, 10: 123-126. 10.1097/00007632-198503000-00002.CrossRef
14.
go back to reference Loncar-Dusek M, Pecina M, Prebeg Z: A longitudinal study of growth velocity and development of secondary gender characteristics versus onset of idiopathic scoliosis. Clin Orthop Relat Res. 1991, 270: 278-282.PubMed Loncar-Dusek M, Pecina M, Prebeg Z: A longitudinal study of growth velocity and development of secondary gender characteristics versus onset of idiopathic scoliosis. Clin Orthop Relat Res. 1991, 270: 278-282.PubMed
15.
go back to reference Duval-Beaupere G: Pathogenic relationship between scoliosis and growth. Scoliosis and Growth. Edited by: Zorab P. 1971, Edinburgh and London: Churchill Livingstone, 58-64. Duval-Beaupere G: Pathogenic relationship between scoliosis and growth. Scoliosis and Growth. Edited by: Zorab P. 1971, Edinburgh and London: Churchill Livingstone, 58-64.
16.
go back to reference Drummond DS, Rogala EJ: Growth and maturation of adolescents with idiopathic scoliosis. Spine (Phila Pa 1976). 1980, 5: 507-511. 10.1097/00007632-198011000-00004.CrossRef Drummond DS, Rogala EJ: Growth and maturation of adolescents with idiopathic scoliosis. Spine (Phila Pa 1976). 1980, 5: 507-511. 10.1097/00007632-198011000-00004.CrossRef
17.
go back to reference Little DG, Song KM, Katz D, Herring JA: Relationship of peak height velocity to other maturity indicators in idiopathic scoliosis in girls. J Bone Joint Surg Am. 2000, 82: 685-693.PubMed Little DG, Song KM, Katz D, Herring JA: Relationship of peak height velocity to other maturity indicators in idiopathic scoliosis in girls. J Bone Joint Surg Am. 2000, 82: 685-693.PubMed
18.
go back to reference Chu WC, Lam WW, Chan YL, Ng BK, Lam TP, Lee KM, Guo X, Cheng JC: Relative shortening and functional tethering of spinal cord in adolescent idiopathic scoliosis?: study with multiplanar reformat magnetic resonance imaging and somatosensory evoked potential. Spine (Phila Pa 1976). 2006, 31: E19-E25. 10.1097/01.brs.0000193892.20764.51.CrossRef Chu WC, Lam WW, Chan YL, Ng BK, Lam TP, Lee KM, Guo X, Cheng JC: Relative shortening and functional tethering of spinal cord in adolescent idiopathic scoliosis?: study with multiplanar reformat magnetic resonance imaging and somatosensory evoked potential. Spine (Phila Pa 1976). 2006, 31: E19-E25. 10.1097/01.brs.0000193892.20764.51.CrossRef
19.
go back to reference Goldberg CJ, Dowling FE, Fogarty EE: Adolescent idiopathic scoliosis--early menarche, normal growth. Spine (Phila Pa 1976). 1993, 18: 529-535. 10.1097/00007632-199304000-00003.CrossRef Goldberg CJ, Dowling FE, Fogarty EE: Adolescent idiopathic scoliosis--early menarche, normal growth. Spine (Phila Pa 1976). 1993, 18: 529-535. 10.1097/00007632-199304000-00003.CrossRef
20.
go back to reference Upadhyay SS, Hsu LC, Ho EK, Leong JC, Lee MK: Disproportionate body growth in girls with adolescent idiopathic scoliosis. A longitudinal study. Spine (Phila Pa 1976). 1991, 16: S343-S347. 10.1097/00007632-199108001-00007.CrossRef Upadhyay SS, Hsu LC, Ho EK, Leong JC, Lee MK: Disproportionate body growth in girls with adolescent idiopathic scoliosis. A longitudinal study. Spine (Phila Pa 1976). 1991, 16: S343-S347. 10.1097/00007632-199108001-00007.CrossRef
21.
go back to reference Acheson RM: The Oxford method of assessing skeletal maturity. Clin Orthop. 1957, 10: 19-39.PubMed Acheson RM: The Oxford method of assessing skeletal maturity. Clin Orthop. 1957, 10: 19-39.PubMed
22.
go back to reference Cobb JR: Scoliosis; quo vadis. J Bone Joint Surg Am. 1958, 40-A: 507-510.PubMed Cobb JR: Scoliosis; quo vadis. J Bone Joint Surg Am. 1958, 40-A: 507-510.PubMed
23.
go back to reference Coonrad RW, Murrell GA, Motley G, Lytle E, Hey LA: A logical coronal pattern classification of 2,000 consecutive idiopathic scoliosis cases based on the scoliosis research society-defined apical vertebra. Spine (Phila Pa 1976). 1998, 23: 1380-1391. 10.1097/00007632-199806150-00016.CrossRef Coonrad RW, Murrell GA, Motley G, Lytle E, Hey LA: A logical coronal pattern classification of 2,000 consecutive idiopathic scoliosis cases based on the scoliosis research society-defined apical vertebra. Spine (Phila Pa 1976). 1998, 23: 1380-1391. 10.1097/00007632-199806150-00016.CrossRef
24.
go back to reference Risser JC: The Iliac apophysis; an invaluable sign in the management of scoliosis. Clin Orthop. 1958, 11: 111-119.PubMed Risser JC: The Iliac apophysis; an invaluable sign in the management of scoliosis. Clin Orthop. 1958, 11: 111-119.PubMed
25.
go back to reference Bitan FD, Veliskakis KP, Campbell BC: Differences in the Risser grading systems in the United States and France. Clin Orthop Relat Res. 2005, 436: 190-195.CrossRefPubMed Bitan FD, Veliskakis KP, Campbell BC: Differences in the Risser grading systems in the United States and France. Clin Orthop Relat Res. 2005, 436: 190-195.CrossRefPubMed
26.
go back to reference Dimeglio A, Canavese F, Charles P: Growth and adolescent idiopathic scoliosis: when and how much?. J Pediatr Orthop. 2011, 31: S28-S36.CrossRefPubMed Dimeglio A, Canavese F, Charles P: Growth and adolescent idiopathic scoliosis: when and how much?. J Pediatr Orthop. 2011, 31: S28-S36.CrossRefPubMed
27.
go back to reference Ballock RT, O’Keefe RJ: The biology of the growth plate. J Bone Joint Surg Am. 2003, 85-A: 715-726.PubMed Ballock RT, O’Keefe RJ: The biology of the growth plate. J Bone Joint Surg Am. 2003, 85-A: 715-726.PubMed
28.
go back to reference Stokes IA, Clark KC, Farnum CE, Aronsson DD: Alterations in the growth plate associated with growth modulation by sustained compression or distraction. Bone. 2007, 41: 197-205. 10.1016/j.bone.2007.04.180.CrossRefPubMedPubMedCentral Stokes IA, Clark KC, Farnum CE, Aronsson DD: Alterations in the growth plate associated with growth modulation by sustained compression or distraction. Bone. 2007, 41: 197-205. 10.1016/j.bone.2007.04.180.CrossRefPubMedPubMedCentral
29.
go back to reference Stokes IA, Spence H, Aronsson DD, Kilmer N: Mechanical modulation of vertebral body growth. Implications for scoliosis progression. Spine (Phila Pa 1976). 1996, 21: 1162-1167. 10.1097/00007632-199605150-00007.CrossRef Stokes IA, Spence H, Aronsson DD, Kilmer N: Mechanical modulation of vertebral body growth. Implications for scoliosis progression. Spine (Phila Pa 1976). 1996, 21: 1162-1167. 10.1097/00007632-199605150-00007.CrossRef
30.
go back to reference Stokes IA, Aronsson DD, Dimock AN, Cortright V, Beck S: Endochondral growth in growth plates of three species at two anatomical locations modulated by mechanical compression and tension. J Orthop Res. 2006, 24: 1327-1334. 10.1002/jor.20189.CrossRefPubMedPubMedCentral Stokes IA, Aronsson DD, Dimock AN, Cortright V, Beck S: Endochondral growth in growth plates of three species at two anatomical locations modulated by mechanical compression and tension. J Orthop Res. 2006, 24: 1327-1334. 10.1002/jor.20189.CrossRefPubMedPubMedCentral
32.
go back to reference Wilsman NJ, Farnum CE, Leiferman EM, Fry M, Barreto C: Differential growth by growth plates as a function of multiple parameters of chondrocytic kinetics. J Orthop Res. 1996, 14: 927-936. 10.1002/jor.1100140613.CrossRefPubMed Wilsman NJ, Farnum CE, Leiferman EM, Fry M, Barreto C: Differential growth by growth plates as a function of multiple parameters of chondrocytic kinetics. J Orthop Res. 1996, 14: 927-936. 10.1002/jor.1100140613.CrossRefPubMed
33.
go back to reference Eerola I, Elima K, Markkula M, Kananen K, Vuorio E: Tissue distribution and phenotypic consequences of different type X collagen gene constructs in transgenic mice. Ann N Y Acad Sci. 1996, 785: 248-250.CrossRefPubMed Eerola I, Elima K, Markkula M, Kananen K, Vuorio E: Tissue distribution and phenotypic consequences of different type X collagen gene constructs in transgenic mice. Ann N Y Acad Sci. 1996, 785: 248-250.CrossRefPubMed
34.
go back to reference Farnum CE, Wilsman NJ: Converting a differentiation cascade into longitudinal growth: stereology and analysis of transgenic animals as tools for understanding growth plate function. Curr Opin Orthop. 2001, 12: 428-433. 10.1097/00001433-200110000-00011.CrossRef Farnum CE, Wilsman NJ: Converting a differentiation cascade into longitudinal growth: stereology and analysis of transgenic animals as tools for understanding growth plate function. Curr Opin Orthop. 2001, 12: 428-433. 10.1097/00001433-200110000-00011.CrossRef
35.
go back to reference Breur GJ, VanEnkevort BA, Farnum CE, Wilsman NJ: Linear relationship between the volume of hypertrophic chondrocytes and the rate of longitudinal bone growth in growth plates. J Orthop Res. 1991, 9: 348-359. 10.1002/jor.1100090306.CrossRefPubMed Breur GJ, VanEnkevort BA, Farnum CE, Wilsman NJ: Linear relationship between the volume of hypertrophic chondrocytes and the rate of longitudinal bone growth in growth plates. J Orthop Res. 1991, 9: 348-359. 10.1002/jor.1100090306.CrossRefPubMed
37.
go back to reference Burwell RG, Aujla RK, Grevitt MP, Randell TL, Dangerfield PH, Cole AA, Kirby AS, Polak FJ, Pratt RK, Webb JK, Moulton A: Upper arm length model suggests transient bilateral asymmetry is associated with right thoracic adolescent idiopathic scoliosis (RT-AIS) with implications for pathogenesis and estimation of linear skeletal overgrowth. Stud Health Technol Inform. 2012, 176: 188-194.PubMed Burwell RG, Aujla RK, Grevitt MP, Randell TL, Dangerfield PH, Cole AA, Kirby AS, Polak FJ, Pratt RK, Webb JK, Moulton A: Upper arm length model suggests transient bilateral asymmetry is associated with right thoracic adolescent idiopathic scoliosis (RT-AIS) with implications for pathogenesis and estimation of linear skeletal overgrowth. Stud Health Technol Inform. 2012, 176: 188-194.PubMed
38.
go back to reference Schwender JD, Denis F: Coronal plane imbalance in adolescent idiopathic scoliosis with left lumbar curves exceeding 40 degrees: the role of the lumbosacral hemicurve. Spine (Phila Pa 1976). 2000, 25: 2358-2363. 10.1097/00007632-200009150-00015.CrossRef Schwender JD, Denis F: Coronal plane imbalance in adolescent idiopathic scoliosis with left lumbar curves exceeding 40 degrees: the role of the lumbosacral hemicurve. Spine (Phila Pa 1976). 2000, 25: 2358-2363. 10.1097/00007632-200009150-00015.CrossRef
39.
go back to reference Burwell RG, Aujla RK, Freeman BJ, Dangerfield PH, Cole AA, Kirby AS, Pratt RK, Webb JK, Moulton A: Patterns of extra-spinal left-right skeletal asymmetries and proximo-distal disproportion in adolescent girls with lower spine scoliosis: ilio-femoral length asymmetry & bilateral tibial/foot length disproportion. Stud Health Technol Inform. 2006, 123: 101-108.PubMed Burwell RG, Aujla RK, Freeman BJ, Dangerfield PH, Cole AA, Kirby AS, Pratt RK, Webb JK, Moulton A: Patterns of extra-spinal left-right skeletal asymmetries and proximo-distal disproportion in adolescent girls with lower spine scoliosis: ilio-femoral length asymmetry & bilateral tibial/foot length disproportion. Stud Health Technol Inform. 2006, 123: 101-108.PubMed
40.
go back to reference Burwell RG, Grevitt MP, Randell TL, Dangerfield PH: In girls with right thoracic adolescent idiopathic scoliosis (RT-AIS) systemic skeletal overgrowth is associated with significant correction in three of four upper limb segments and not in lower limb segments. Clin Anat. 2012, 25: 2-10.1002/ca.22007.CrossRef Burwell RG, Grevitt MP, Randell TL, Dangerfield PH: In girls with right thoracic adolescent idiopathic scoliosis (RT-AIS) systemic skeletal overgrowth is associated with significant correction in three of four upper limb segments and not in lower limb segments. Clin Anat. 2012, 25: 2-10.1002/ca.22007.CrossRef
41.
go back to reference Nicolopoulos KS, Burwell RG, Webb JK: Stature and its components in adolescent idiopathic scoliosis. Cephalo-caudal disproportion in the trunk of girls. J Bone Joint Surg Br. 1985, 67: 594-601.PubMed Nicolopoulos KS, Burwell RG, Webb JK: Stature and its components in adolescent idiopathic scoliosis. Cephalo-caudal disproportion in the trunk of girls. J Bone Joint Surg Br. 1985, 67: 594-601.PubMed
Metadata
Title
Accelerated endochondral growth in adolescents with idiopathic scoliosis: a preliminary histomorphometric study
Authors
Xin Zheng
Weijun Wang
Bangping Qian
Shoufeng Wang
Zezhang Zhu
Bin Wang
Xu Sun
Yitao Ding
Yong Qiu
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2014
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/1471-2474-15-429

Other articles of this Issue 1/2014

BMC Musculoskeletal Disorders 1/2014 Go to the issue