Asian Spine Journal

Korean Society of Spine Surgery (대한척추외과학회)
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The Role of Vitamin D in the Pathogenesis of Adolescent Idiopathic Scoliosis

  • Received : 2017.12.18
  • Accepted : 2018.05.22
  • Published : 2018.12.31
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Abstract

Several theories have been proposed to explain the etiology of adolescent idiopathic scoliosis (AIS) until present. However, limited data are available regarding the impact of vitamin D insufficiency or deficiency on scoliosis. Previous studies have shown that vitamin D deficiency and insufficiency are prevalent in adolescents, including AIS patients. A series of studies conducted in Hong Kong have shown that as many as 30% of these patients have osteopenia. The 25-hydroxyvitamin D3 level has been found to positively correlate with bone mineral density (BMD) in healthy adolescents and negatively with Cobb angle in AIS patients; therefore, vitamin D deficiency is believed to play a role in AIS pathogenesis. This study attempts to review the relevant literature on AIS etiology to examine the association of vitamin D and various current theories. Our review suggested that vitamin D deficiency is associated with several current etiological theories of AIS. We postulate that vitamin D deficiency and/or insufficiency affects AIS development by its effect on the regulation of fibrosis, postural control, and BMD. Subclinical deficiency of vitamin K2, a fat-soluble vitamin, is also prevalent in adolescents; therefore, it is possible that the high prevalence of vitamin D deficiency is related to decreased fat intake. Further studies are required to elucidate the possible role of vitamin D in the pathogenesis and clinical management of AIS.

Keywords

References

  1. Konieczny MR, Senyurt H, Krauspe R. Epidemiology of adolescent idiopathic scoliosis. J Child Orthop 2013;7:3-9. https://doi.org/10.1007/s11832-012-0457-4
  2. Burwell RG, Dangerfield PH, Freeman BJ. Concepts on the pathogenesis of adolescent idiopathic scoliosis: bone growth and mass, vertebral column, spinal cord, brain, skull, extra-spinal left-right skeletal length asymmetries, disproportions and molecular pathogenesis. Stud Health Technol Inform 2008;135:3-52.
  3. Cheng JC, Guo X, Sher AH. Persistent osteopenia in adolescent idiopathic scoliosis: a longitudinal follow up study. Spine (Phila Pa 1976) 1999;24:1218-22. https://doi.org/10.1097/00007632-199906150-00008
  4. Lee WT, Cheung CS, Tse YK, et al. Association of osteopenia with curve severity in adolescent idiopathic scoliosis: a study of 919 girls. Osteoporos Int 2005;16:1924-32. https://doi.org/10.1007/s00198-005-1964-7
  5. Hung VW, Qin L, Cheung CS, et al. Osteopenia: a new prognostic factor of curve progression in adolescent idiopathic scoliosis. J Bone Joint Surg Am 2005;87:2709-16.
  6. Schlosser TP, van der Heijden GJ, Versteeg AL, Castelein RM. How 'idiopathic' is adolescent idiopathic scoliosis?: a systematic review on associated abnormalities. PLoS One 2014;9:e97461. https://doi.org/10.1371/journal.pone.0097461
  7. Akdeniz S, Hepguler S, Ozturk C, Atamaz FC. The relation between vitamin D and postural balance according to clinical tests and tetrax posturography. J Phys Ther Sci 2016;28:1272-7. https://doi.org/10.1589/jpts.28.1272
  8. Viapiana O, Gatti D, Rossini M, Idolazzi L, Fracassi E, Adami S. Vitamin D and fractures: a systematic review. Reumatismo 2007;59:15-9.
  9. Gatti D, El Ghoch M, Viapiana O, et al. Strong relationship between vitamin D status and bone mineral density in anorexia nervosa. Bone 2015;78:212-5. https://doi.org/10.1016/j.bone.2015.05.014
  10. Balioglu MB, Aydin C, Kargin D, et al. Vitamin-D measurement in patients with adolescent idiopathic scoliosis. J Pediatr Orthop B 2017;26:48-52. https://doi.org/10.1097/BPB.0000000000000320
  11. Wynne-Davies R. Familial (idiopathic) scoliosis: a family survey. J Bone Joint Surg Br 1968;50:24-30.
  12. Riseborough EJ, Wynne-Davies R. A genetic survey of idiopathic scoliosis in Boston, Massachusetts. J Bone Joint Surg Am 1973;55:974-82. https://doi.org/10.2106/00004623-197355050-00006
  13. Tang NL, Yeung HY, Hung VW, et al. Genetic epidemiology and heritability of AIS: a study of 415 Chinese female patients. J Orthop Res 2012;30:1464-9. https://doi.org/10.1002/jor.22090
  14. Favaro D. Genetic pathway analysis of adolescent idiopathic scoliosis [bachelor's thesis]. Meadville (PA): Allegheny College; 2017.
  15. Wang K, Li M, Hakonarson H. Analysing biological pathways in genome-wide association studies. Nat Rev Genet 2010;11:843-54. https://doi.org/10.1038/nrg2884
  16. Manolio TA. Bringing genome-wide association findings into clinical use. Nat Rev Genet 2013;14:549-58.
  17. Moore TJ, Furberg CD. The safety risks of innovation: the FDA's Expedited Drug Development Pathway. JAMA 2012;308:869-70. https://doi.org/10.1001/jama.2012.9658
  18. Kutmon M, Rieswijk L. Spinal cord injury (bos taurus) [Internet]. San Francisco (CA): WikiPathways; 2016 [cited 2017 Sep 30]. Available from: http://www.wikipathways.org/index.php/Pathway:WP3186.
  19. Teitelbaum SL, Bone JM, Stein PM, et al. Calcifediol in chronic renal insufficiency: skeletal response. JAMA 1976;235:164-7. https://doi.org/10.1001/jama.1976.03260280022019
  20. Barchetta I. Could vitamin d supplementation benefit patients with chronic liver disease? Gastroenterol Hepatol (N Y) 2012;8:755-7.
  21. Zhang Z, Yu X, Fang X, et al. Preventive effects of vitamin D treatment on bleomycin-induced pulmonary fibrosis. Sci Rep 2015;5:17638. https://doi.org/10.1038/srep17638
  22. Ramirez AM, Wongtrakool C, Welch T, Steinmeyer A, Zugel U, Roman J. Vitamin D inhibition of profibrotic effects of transforming growth factor beta1 in lung fibroblasts and epithelial cells. J Steroid Biochem Mol Biol 2010;118:142-50. https://doi.org/10.1016/j.jsbmb.2009.11.004
  23. Zhang GY, Cheng T, Luan Q, et al. Vitamin D: a novel therapeutic approach for keloid, an in vitro analysis. Br J Dermatol 2011;164:729-37. https://doi.org/10.1111/j.1365-2133.2010.10130.x
  24. Abe K, Inage K, Sakuma Y, et al. Evaluation of histological changes in back muscle injuries in rats over time. Asian Spine J 2017;11:88-92. https://doi.org/10.4184/asj.2017.11.1.88
  25. Li Q, Chen J, Chen Y, Cong X, Chen Z. Chronic sciatic nerve compression induces fibrosis in dorsal root ganglia. Mol Med Rep 2016;13:2393-400. https://doi.org/10.3892/mmr.2016.4810
  26. Boyan BD, Schwartz Z, Swain LD. In vitro studies on the regulation of endochondral ossification by vitamin D. Crit Rev Oral Biol Med 1992;3:15-30. https://doi.org/10.1177/10454411920030010401
  27. Dziewiatkowski DD. Vitamin D and endochondral ossification in the rat as indicated by the use of sulfur-35 and phosphorus-32. J Exp Med 1954;100:25-32. https://doi.org/10.1084/jem.100.1.25
  28. Moldovan F, Hassan A, Bagu E, Zaouter C, Patten SA. Could estrogen impact a new pertinent gene for AIS? Scoliosis 2015;10(Suppl 1):O2. https://doi.org/10.1186/1748-7161-10-S1-O2.
  29. Leboeuf D, Letellier K, Alos N, Edery P, Moldovan F. Do estrogens impact adolescent idiopathic scoliosis? Trends Endocrinol Metab 2009;20:147-52. https://doi.org/10.1016/j.tem.2008.12.004
  30. Kinuta K, Tanaka H, Moriwake T, Aya K, Kato S, Seino Y. Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads. Endocrinology 2000;141:1317-24. https://doi.org/10.1210/endo.141.4.7403
  31. Halloran BP, DeLuca HF. Effect of vitamin D deficiency on fertility and reproductive capacity in the female rat. J Nutr 1980;110:1573-80. https://doi.org/10.1093/jn/110.8.1573
  32. Knight JA, Wong J, Blackmore KM, Raboud JM, Vieth R. Vitamin D association with estradiol and progesterone in young women. Cancer Causes Control 2010;21:479-83. https://doi.org/10.1007/s10552-009-9466-0
  33. Arai S, Ohtsuka Y, Moriya H, Kitahara H, Minami S. Scoliosis associated with syringomyelia. Spine (Phila Pa 1976) 1993;18:1591-2. https://doi.org/10.1097/00007632-199309000-00004
  34. Isu T, Chono Y, Iwasaki Y, et al. Scoliosis associated with syringomyelia presenting in children. Childs Nerv Syst 1992;8:97-100. https://doi.org/10.1007/BF00298449
  35. Cheng JC, Chau WW, Guo X, Chan YL. Redefining the magnetic resonance imaging reference level for the cerebellar tonsil: a study of 170 adolescents with normal versus idiopathic scoliosis. Spine (Phila Pa 1976) 2003;28:815-8.
  36. Chu WC, Man GC, Lam WW, et al. A detailed morphologic and functional magnetic resonance imaging study of the craniocervical junction in adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 2007;32:1667-74. https://doi.org/10.1097/BRS.0b013e318074d539
  37. Sun X, Qiu Y, Zhu Z, et al. Variations of the position of the cerebellar tonsil in idiopathic scoliotic adolescents with a cobb angle >40 degrees: a magnetic resonance imaging study. Spine (Phila Pa 1976) 2007;32:1680-6. https://doi.org/10.1097/BRS.0b013e318074d3f5
  38. Dretakis EK. Brain-stem dysfunction and idiopathic scoliosis. Stud Health Technol Inform 2002;91:422-7.
  39. Geissele AE, Kransdorf MJ, Geyer CA, Jelinek JS, Van Dam BE. Magnetic resonance imaging of the brain stem in adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 1991;16:761-3. https://doi.org/10.1097/00007632-199107000-00013
  40. Chu WC, Shi L, Wang D, et al. Variations of semicircular canals orientation and left-right asymmetry in adolescent idiopathic scoliosis (AIS) comparing with normal controls: MR morphometry study using advanced image computation techniques. Stud Health Technol Inform 2008;140;333.
  41. Simoneau M, Richer N, Mercier P, Allard P, Teasdale N. Sensory deprivation and balance control in idiopathic scoliosis adolescent. Exp Brain Res 2006;170:576-82. https://doi.org/10.1007/s00221-005-0246-0
  42. Barrack RL, Wyatt MP, Whitecloud TS 3rd, Burke SW, Roberts JM, Brinker MR. Vibratory hypersensitivity in idiopathic scoliosis. J Pediatr Orthop 1988;8:389-95. https://doi.org/10.1097/01241398-198807000-00002
  43. Wiener-Vacher SR, Mazda K. Asymmetric otolith vestibulo-ocular responses in children with idiopathic scoliosis. J Pediatr 1998;132:1028-32. https://doi.org/10.1016/S0022-3476(98)70403-2
  44. Pialasse JP, Descarreaux M, Mercier P, Blouin J, Simoneau M. The vestibular-evoked postural response of adolescents with idiopathic scoliosis is altered. PLoS One 2015;10:e0143124. https://doi.org/10.1371/journal.pone.0143124
  45. Guo X, Chau WW, Hui-Chan CW, Cheung CS, Tsang WW, Cheng JC. Balance control in adolescents with idiopathic scoliosis and disturbed somatosensory function. Spine (Phila Pa 1976) 2006;31:E437-40. https://doi.org/10.1097/01.brs.0000222048.47010.bf
  46. Lao ML, Chow DH, Guo X, Cheng JC, Holmes AD. Impaired dynamic balance control in adolescents with idiopathic scoliosis and abnormal somatosensory evoked potentials. J Pediatr Orthop 2008;28:846-9. https://doi.org/10.1097/BPO.0b013e31818e1bc9
  47. Beaulieu M, Toulotte C, Gatto L, et al. Postural imbalance in non-treated adolescent idiopathic scoliosis at different periods of progression. Eur Spine J 2009;18:38-44. https://doi.org/10.1007/s00586-008-0831-6
  48. Veldhuizen AG, Wever DJ, Webb PJ. The aetiology of idiopathic scoliosis: biomechanical and neuromuscular factors. Eur Spine J 2000;9:178-84. https://doi.org/10.1007/s005860000142
  49. Haumont T, Gauchard GC, Lascombes P, Perrin PP. Postural instability in early-stage idiopathic scoliosis in adolescent girls. Spine (Phila Pa 1976) 2011;36:E847-54. https://doi.org/10.1097/BRS.0b013e3181ff5837
  50. McGrath JJ, Feron FP, Burne TH, Mackay-Sim A, Eyles DW. Vitamin D3-implications for brain development. J Steroid Biochem Mol Biol 2004;89-90:557-60. https://doi.org/10.1016/j.jsbmb.2004.03.070
  51. Hawes JE, Tesic D, Whitehouse AJ, Zosky GR, Smith JT, Wyrwoll CS. Maternal vitamin D deficiency alters fetal brain development in the BALB/c mouse. Behav Brain Res 2015;286:192-200. https://doi.org/10.1016/j.bbr.2015.03.008
  52. Cui X, Gooch H, Petty A, McGrath JJ, Eyles D. Vitamin D and the brain: genomic and non-genomic actions. Mol Cell Endocrinol 2017;453:131-43. https://doi.org/10.1016/j.mce.2017.05.035
  53. Stumpf WE, Sar M, Reid FA, Tanaka Y, DeLuca HF. Target cells for 1,25-dihydroxyvitamin D3 in intestinal tract, stomach, kidney, skin, pituitary, and parathyroid. Science 1979;206:1188-90. https://doi.org/10.1126/science.505004
  54. Stumpf WE, Sar M, Narbaitz R, Reid FA, DeLuca HF, Tanaka Y. Cellular and subcellular localization of 1,25-(OH)2-vitamin D3 in rat kidney: comparison with localization of parathyroid hormone and estradiol. Proc Natl Acad Sci U S A 1980;77:1149-53. https://doi.org/10.1073/pnas.77.2.1149
  55. Stumpf WE, O'Brien LP. 1,25 (OH)2 vitamin D3 sites of action in the brain: an autoradiographic study. Histochemistry 1987;87:393-406. https://doi.org/10.1007/BF00496810
  56. Eyles D, Brown J, Mackay-Sim A, McGrath J, Feron F. Vitamin D3 and brain development. Neuroscience 2003;118:641-53. https://doi.org/10.1016/S0306-4522(03)00040-X
  57. Feron F, Burne TH, Brown J, et al. Developmental vitamin D3 deficiency alters the adult rat brain. Brain Res Bull 2005;65:141-8. https://doi.org/10.1016/j.brainresbull.2004.12.007
  58. Annweiler C, Montero-Odasso M, Hachinski V, Seshadri S, Bartha R, Beauchet O. Vitamin D concentration and lateral cerebral ventricle volume in older adults. Mol Nutr Food Res 2013;57:267-76. https://doi.org/10.1002/mnfr.201200418
  59. Annweiler C, Beauchet O, Bartha R, Hachinski V, Montero-Odasso M; WALK Team (Working group Angers-London for Knowledge). Vitamin D and caudal primary motor cortex: a magnetic resonance spectroscopy study. PLoS One 2014;9:e87314. https://doi.org/10.1371/journal.pone.0087314
  60. Eyles DW, Smith S, Kinobe R, Hewison M, McGrath JJ. Distribution of the vitamin D receptor and 1 alpha-hydroxylase in human brain. J Chem Neuroanat 2005;29:21-30. https://doi.org/10.1016/j.jchemneu.2004.08.006
  61. Gezen-Ak D, Dursun E, Yilmazer S. Vitamin D inquiry in hippocampal neurons: consequences of vitamin D-VDR pathway disruption on calcium channel and the vitamin D requirement. Neurol Sci 2013;34:1453-8. https://doi.org/10.1007/s10072-012-1268-6
  62. Perez-Fernandez R, Alonso M, Segura C, et al. Vitamin D receptor gene expression in human pituitary gland. Life Sci 1997;60:35-42.
  63. Kuether TA, Piatt JH. Chiari malformation associated with vitamin D-resistant rickets: case report. Neurosurgery 1998;42:1168-71. https://doi.org/10.1097/00006123-199805000-00134
  64. Zhang W, Sha S, Xu L, Liu Z, Qiu Y, Zhu Z. The prevalence of intraspinal anomalies in infantile and juvenile patients with “presumed idiopathic” scoliosis: a MRI-based analysis of 504 patients. BMC Musculoskelet Disord 2016;17:189. https://doi.org/10.1186/s12891-016-1026-7
  65. Minasyan A, Keisala T, Zou J, et al. Vestibular dysfunction in vitamin D receptor mutant mice. J Steroid Biochem Mol Biol 2009;114:161-6. https://doi.org/10.1016/j.jsbmb.2009.01.020
  66. Beauchet O, Annweiler C, Verghese J, Fantino B, Herrmann FR, Allali G. Biology of gait control: vitamin D involvement. Neurology 2011;76:1617-22. https://doi.org/10.1212/WNL.0b013e318219fb08
  67. Krause M, Anschutz W, Vettorazzi E, Breer S, Amling M, Barvencik F. Vitamin D deficiency intensifies deterioration of risk factors, such as male sex and absence of vision, leading to increased postural body sway. Gait Posture 2014;39:166-71. https://doi.org/10.1016/j.gaitpost.2013.06.017
  68. Kalueff AV, Lou YR, Laaksi I, Tuohimaa P. Impaired motor performance in mice lacking neurosteroid vitamin D receptors. Brain Res Bull 2004;64:25-9. https://doi.org/10.1016/j.brainresbull.2004.04.015
  69. Anek A, Bunyaratavej N, Jittivilai T. Effects of shortterm vitamin D supplementation on musculoskeletal and body balance for prevention of falling in postmenopausal women. J Med Assoc Thai 2015;98 Suppl 8:S26-31.
  70. Cangussu LM, Nahas-Neto J, Orsatti CL, et al. Effect of isolated vitamin D supplementation on the rate of falls and postural balance in postmenopausal women fallers: a randomized, double-blind, placebocontrolled trial. Menopause 2016;23:267-74. https://doi.org/10.1097/GME.0000000000000525
  71. Saito K, Miyakoshi N, Matsunaga T, Hongo M, Kasukawa Y, Shimada Y. Eldecalcitol improves muscle strength and dynamic balance in postmenopausal women with osteoporosis: an open-label randomized controlled study. J Bone Miner Metab 2016;34:547-54. https://doi.org/10.1007/s00774-015-0695-x
  72. Sanyelbhaa H, Sanyelbhaa A. Vestibular-evoked myogenic potentials and subjective visual vertical testing in patients with vitamin D deficiency/insufficiency. Eur Arch Otorhinolaryngol 2015;272:3233-9. https://doi.org/10.1007/s00405-014-3395-6
  73. Nordwall A, Willner S. A study of skeletal age and height in girls with idiopathic scoliosis. Clin Orthop Relat Res 1975;(110):6-10.
  74. Archer IA, Dickson RA. Stature and idiopathic scoliosis: a prospective study. J Bone Joint Surg Br 1985;67:185-8.
  75. 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.
  76. Ylikoski M. Height of girls with adolescent idiopathic scoliosis. Eur Spine J 2003;12:288-91.
  77. Goldberg CJ, Dowling FE, Fogarty EE. Adolescent idiopathic scoliosis: early menarche, normal growth. Spine (Phila Pa 1976) 1993;18:529-35. https://doi.org/10.1097/00007632-199304000-00003
  78. Kitagawa I, Kitagawa Y, Kawase Y, Nagaya T, Tokudome S. Advanced onset of menarche and higher bone mineral density depending on vitamin D receptor gene polymorphism. Eur J Endocrinol 1998;139:522-7. https://doi.org/10.1530/eje.0.1390522
  79. Ylikoski M, Peltonen J, Poussa M. Biological factors and predictability of bracing in adolescent idiopathic scoliosis. J Pediatr Orthop 1989;9:680-3. https://doi.org/10.1097/01241398-198911000-00009
  80. Siu King Cheung C, Tak Keung Lee W, Kit Tse Y, et al. Abnormal peri-pubertal anthropometric measurements and growth pattern in adolescent idiopathic scoliosis: a study of 598 patients. Spine (Phila Pa 1976) 2003;28:2152-7. https://doi.org/10.1097/01.BRS.0000084265.15201.D5
  81. Warren MP, Brooks-Gunn J, Hamilton LH, Warren LF, Hamilton WG. Scoliosis and fractures in young ballet dancers: relation to delayed menarche and secondary amenorrhea. N Engl J Med 1986;314:1348-53. https://doi.org/10.1056/NEJM198605223142104
  82. Mao SH, Jiang J, Sun X, et al. Timing of menarche in Chinese girls with and without adolescent idiopathic scoliosis: current results and review of the literature. Eur Spine J 2011;20:260-5. https://doi.org/10.1007/s00586-010-1649-6
  83. Yim AP, Yeung HY, Hung VW, et al. Abnormal skeletal growth patterns in adolescent idiopathic scoliosis: a longitudinal study until skeletal maturity. Spine (Phila Pa 1976) 2012;37:E1148-54. https://doi.org/10.1097/BRS.0b013e31825c036d
  84. Janusz P, Kotwicka M, Andrusiewicz M, Czaprowski D, Czubak J, Kotwicki T. Estrogen receptors genes polymorphisms and age at menarche in idiopathic scoliosis. BMC Musculoskelet Disord 2014;15:383. https://doi.org/10.1186/1471-2474-15-383
  85. Treloar SA, Martin NG. Age at menarche as a fitness trait: nonadditive genetic variance detected in a large twin sample. Am J Hum Genet 1990;47:137-48.
  86. Villamor E, Marin C, Mora-Plazas M, Baylin A. Vitamin D deficiency and age at menarche: a prospective study. Am J Clin Nutr 2011;94:1020-5. https://doi.org/10.3945/ajcn.111.018168
  87. Grivas TB, Vasiliadis E, Mouzakis V, Mihas C, Koufopoulos G. Association between adolescent idiopathic scoliosis prevalence and age at menarche in different geographic latitudes. Scoliosis 2006;1:9. https://doi.org/10.1186/1748-7161-1-9
  88. Dossus L, Kvaskoff M, Bijon A, et al. Latitude and ultraviolet radiation dose in the birthplace in relation to menarcheal age in a large cohort of French women. Int J Epidemiol 2013;42:590-600. https://doi.org/10.1093/ije/dyt007
  89. Sohn K. The influence of climate on age at menarche: augmented with the influence of ancestry. Homo 2016;67:328-36. https://doi.org/10.1016/j.jchb.2016.06.001
  90. Hagenau T, Vest R, Gissel TN, et al. Global vitamin D levels in relation to age, gender, skin pigmentation and latitude: an ecologic meta-regression analysis. Osteoporos Int 2009;20:133-40. https://doi.org/10.1007/s00198-008-0626-y
  91. Yermachenko A, Dvornyk V. Nongenetic determinants of age at menarche: a systematic review. Biomed Res Int 2014;2014:371583.
  92. Lundqvist J. Vitamin D as a regulator of steroidogenic enzymes. F1000Research 2014;3:155. https://doi.org/10.12688/f1000research.4714.1.
  93. Krishnan AV, Swami S, Feldman D. Vitamin D and breast cancer: inhibition of estrogen synthesis and signaling. J Steroid Biochem Mol Biol 2010;121:343-8. https://doi.org/10.1016/j.jsbmb.2010.02.009
  94. Yu WS, Chan KY, Yu FW, et al. Bone structural and mechanical indices in adolescent idiopathic scoliosis evaluated by high-resolution peripheral quantitative computed tomography (HR-pQCT). Bone 2014;61:109-15. https://doi.org/10.1016/j.bone.2013.12.033
  95. Cheng JC, Qin L, Cheung CS, et al. Generalized low areal and volumetric bone mineral density in adolescent idiopathic scoliosis. J Bone Miner Res 2000;15:1587-95. https://doi.org/10.1359/jbmr.2000.15.8.1587
  96. Cheung TF, Cheuk KY, Yu FW, et al. Prevalence of vitamin D insufficiency among adolescents and its correlation with bone parameters using highresolution peripheral quantitative computed tomography. Osteoporos Int 2016;27:2477-88. https://doi.org/10.1007/s00198-016-3552-4
  97. Burner WL 3rd, Badger VM, Sherman FC. Osteoporosis and acquired back deformities. J Pediatr Orthop 1982;2:383-5. https://doi.org/10.1097/01241398-198210000-00006
  98. Velis KP, Healey JH, Schneider R. Osteoporosis in unstable adult scoliosis. Clin Orthop Relat Res 1988;(237):132-41.
  99. Cheng JC, Guo X. Osteopenia in adolescent idiopathic scoliosis: a primary problem or secondary to the spinal deformity? Spine (Phila Pa 1976) 1997;22:1716-21. https://doi.org/10.1097/00007632-199708010-00006
  100. Yip BH, Yu FW, Wang Z, et al. Prognostic value of bone mineral density on curve progression: a longitudinal cohort study of 513 girls with adolescent idiopathic scoliosis. Sci Rep 2016;6:39220. https://doi.org/10.1038/srep39220
  101. Wang ZW, Lee WY, Lam TP, et al. Defining the bone morphometry, micro-architecture and volumetric density profile in osteopenic vs non-osteopenic adolescent idiopathic scoliosis. Eur Spine J 2017;26:1586-94. https://doi.org/10.1007/s00586-016-4422-7
  102. Tam EM, Yu FW, Hung VW, et al. Are volumetric bone mineral density and bone micro-architecture associated with leptin and soluble leptin receptor levels in adolescent idiopathic scoliosis?: a casecontrol study. PLoS One 2014;9:e87939. https://doi.org/10.1371/journal.pone.0087939
  103. Suh KT, Lee SS, Hwang SH, Kim SJ, Lee JS. Elevated soluble receptor activator of nuclear factor-kappaB ligand and reduced bone mineral density in patients with adolescent idiopathic scoliosis. Eur Spine J 2007;16:1563-9. https://doi.org/10.1007/s00586-007-0390-2
  104. Silva RT, Fernandes RJ, Ono AH, Marcon RM, Cristante AF, de Barros Filho TE. Role of different hormones in the pathogenesis and severity of adolescent idiopathic scoliosis. Acta Ortop Bras 2017;25:15-7. https://doi.org/10.1590/1413-785220172501168600
  105. Lehtonen-Veromaa MK, Mottonen TT, Nuotio IO, Irjala KM, Leino AE, Viikari JS. Vitamin D and attainment of peak bone mass among peripubertal Finnish girls: a 3-y prospective study. Am J Clin Nutr 2002;76:1446-53. https://doi.org/10.1093/ajcn/76.6.1446
  106. Zhu K, Oddy WH, Holt P, et al. Tracking of vitamin D status from childhood to early adulthood and its association with peak bone mass. Am J Clin Nutr 2017;106:276-83. https://doi.org/10.3945/ajcn.116.150524
  107. Cashman KD, Hill TR, Cotter AA, et al. Low vitamin D status adversely affects bone health parameters in adolescents. Am J Clin Nutr 2008;87:1039-44. https://doi.org/10.1093/ajcn/87.4.1039
  108. Sayers A, Fraser WD, Lawlor DA, Tobias JH. 25-Hydroxyvitamin-D3 levels are positively related to subsequent cortical bone development in childhood: findings from a large prospective cohort study. Osteoporos Int 2012;23:2117-28. https://doi.org/10.1007/s00198-011-1813-9
  109. Fox KM, Magaziner J, Sherwin R, et al. Reproductive correlates of bone mass in elderly women: study of Osteoporotic Fractures Research Group. J Bone Miner Res 1993;8:901-8.
  110. Tuppurainen M, Kroger H, Saarikoski S, Honkanen R, Alhava E. The effect of gynecological risk factors on lumbar and femoral bone mineral density in peri- and postmenopausal women. Maturitas 1995;21:137-45. https://doi.org/10.1016/0378-5122(94)00878-B
  111. Gerdhem P, Obrant KJ. Bone mineral density in old age: the influence of age at menarche and menopause. J Bone Miner Metab 2004;22:372-5.
  112. Apter D, Vihko R. Premenarcheal endocrine changes in relation to age at menarche. Clin Endocrinol (Oxf) 1985;22:753-60. https://doi.org/10.1111/j.1365-2265.1985.tb00165.x
  113. Chang HK, Chang DG, Myong JP, et al. Bone mineral density among Korean females aged 20- 50 years: influence of age at menarche (The Korea National Health and Nutrition Examination Survey 2008-2011). Osteoporos Int 2017;28:2129-36. https://doi.org/10.1007/s00198-017-3997-0
  114. Ho AY, Kung AW. Determinants of peak bone mineral density and bone area in young women. J Bone Miner Metab 2005;23:470-5. https://doi.org/10.1007/s00774-005-0630-7
  115. Chevalley T, Bonjour JP, Ferrari S, Rizzoli R. Influence of age at menarche on forearm bone microstructure in healthy young women. J Clin Endocrinol Metab 2008;93:2594-601. https://doi.org/10.1210/jc.2007-2644
  116. Kulis A, Zarzycki D, Jaskiewicz J. Concentration of estradiol in girls with idiophatic scoliosis. Ortop Traumatol Rehabil 2006;8:455-9.
  117. Esposito T, Uccello R, Caliendo R, et al. Estrogen receptor polymorphism, estrogen content and idiopathic scoliosis in human: a possible genetic linkage. J Steroid Biochem Mol Biol 2009;116:56-60. https://doi.org/10.1016/j.jsbmb.2009.04.010
  118. Man GC, Wong JH, Wang WW, et al. Abnormal melatonin receptor 1B expression in osteoblasts from girls with adolescent idiopathic scoliosis. J Pineal Res 2011;50:395-402. https://doi.org/10.1111/j.1600-079X.2011.00857.x
  119. Chen C, Xu C, Zhou T, et al. Abnormal osteogenic and chondrogenic differentiation of human mesenchymal stem cells from patients with adolescent idiopathic scoliosis in response to melatonin. Mol Med Rep 2016;14:1201-9. https://doi.org/10.3892/mmr.2016.5384
  120. Clark EM, Taylor HJ, Harding I, et al. Association between components of body composition and scoliosis: a prospective cohort study reporting differences identifiable before the onset of scoliosis. J Bone Miner Res 2014;29:1729-36. https://doi.org/10.1002/jbmr.2207
  121. Burwell RG, Clark EM, Dangerfield PH, Moulton A. Adolescent idiopathic scoliosis (AIS): a multifactorial cascade concept for pathogenesis and embryonic origin. Scoliosis Spinal Disord 2016;11:8. https://doi.org/10.1186/s13013-016-0063-1
  122. Weinstein SL, Dolan LA, Cheng JC, Danielsson A, Morcuende JA. Adolescent idiopathic scoliosis. Lancet 2008;371:1527-37. https://doi.org/10.1016/S0140-6736(08)60658-3
  123. Raczkowski JW. The concentrations of testosterone and estradiol in girls with adolescent idiopathic scoliosis. Neuro Endocrinol Lett 2007;28:302-4.
  124. Sanders JO, Browne RH, McConnell SJ, Margraf SA, Cooney TE, Finegold DN. Maturity assessment and curve progression in girls with idiopathic scoliosis. J Bone Joint Surg Am 2007;89:64-73. https://doi.org/10.2106/JBJS.F.00067
  125. Kulis A, Gozdzialska A, Drag J, et al. Participation of sex hormones in multifactorial pathogenesis of adolescent idiopathic scoliosis. Int Orthop 2015;39:1227-36. https://doi.org/10.1007/s00264-015-2742-6
  126. Cutler GB Jr. The role of estrogen in bone growth and maturation during childhood and adolescence. J Steroid Biochem Mol Biol 1997;61:141-4. https://doi.org/10.1016/S0960-0760(97)80005-2
  127. Letellier K, Azeddine B, Parent S, et al. Estrogen cross-talk with the melatonin signaling pathway in human osteoblasts derived from adolescent idiopathic scoliosis patients. J Pineal Res 2008;45:383-93. https://doi.org/10.1111/j.1600-079X.2008.00603.x
  128. Del Rio B, Garcia Pedrero JM, Martinez-Campa C, et al. Melatonin, an endogenous-specific inhibitor of estrogen receptor alpha via calmodulin. J Biol Chem 2004;279:38294-302. https://doi.org/10.1074/jbc.M403140200
  129. Sanchez-Barcelo EJ, Mediavilla MD, Tan DX, Reiter RJ. Scientific basis for the potential use of melatonin in bone diseases: osteoporosis and adolescent idiopathic scoliosis. J Osteoporos 2010;2010:830231.
  130. Gallagher JC, Riggs BL, DeLuca HF. Effect of estrogen on calcium absorption and serum vitamin D metabolites in postmenopausal osteoporosis. J Clin Endocrinol Metab 1980;51:1359-64. https://doi.org/10.1210/jcem-51-6-1359
  131. Gilad LA, Bresler T, Gnainsky J, Smirnoff P, Schwartz B. Regulation of vitamin D receptor expression via estrogen-induced activation of the ERK 1/2 signaling pathway in colon and breast cancer cells. J Endocrinol 2005;185:577-92. https://doi.org/10.1677/joe.1.05770
  132. Davoodi F, Brenner RV, Evans SR, et al. Modulation of vitamin D receptor and estrogen receptor by 1,25(OH)2-vitamin D3 in T-47D human breast cancer cells. J Steroid Biochem Mol Biol 1995;54:147-53. https://doi.org/10.1016/0960-0760(95)00128-M
  133. Xu H, Long JR, Li MX, Deng HW. Interaction effects between estrogen receptor alpha and vitamin D receptor genes on age at menarche in Chinese women. Acta Pharmacol Sin 2005;26:860-4. https://doi.org/10.1111/j.1745-7254.2005.00122.x
  134. Willing M, Sowers M, Aron D, et al. Bone mineral density and its change in white women: estrogen and vitamin D receptor genotypes and their interaction. J Bone Miner Res 1998;13:695-705. https://doi.org/10.1359/jbmr.1998.13.4.695
  135. Machida M, Murai I, Miyashita Y, Dubousset J, Yamada T, Kimura J. Pathogenesis of idiopathic scoliosis: experimental study in rats. Spine (Phila Pa 1976) 1999;24:1985-9. https://doi.org/10.1097/00007632-199910010-00004
  136. Dubousset J, Machida M. Possible role of the pineal gland in the pathogenesis of idiopathic scoliosis: experimental and clinical studies. Bull Acad Natl Med 2001;185:593-602.
  137. Brodner W, Krepler P, Nicolakis M, et al. Melatonin and adolescent idiopathic scoliosis. J Bone Joint Surg Br 2000;82:399-403. https://doi.org/10.1302/0301-620X.82B3.0820399
  138. Cheung KM, Wang T, Poon AM, et al. The effect of pinealectomy on scoliosis development in young nonhuman primates. Spine (Phila Pa 1976) 2005;30:2009-13. https://doi.org/10.1097/01.brs.0000179087.38730.5d
  139. Yang S, Zheng C, Jiang J, et al. The value of applying a melatonin antagonist (Luzindole) in improving the success rate of the bipedal rat scoliosis model. BMC Musculoskelet Disord 2017;18:137. https://doi.org/10.1186/s12891-017-1500-x
  140. Azeddine B, Letellier K, Wang da S, Moldovan F, Moreau A. Molecular determinants of melatonin signaling dysfunction in adolescent idiopathic scoliosis. Clin Orthop Relat Res 2007;462:45-52. https://doi.org/10.1097/BLO.0b013e31811f39fa
  141. Nakade O, Koyama H, Ariji H, Yajima A, Kaku T. Melatonin stimulates proliferation and type I collagen synthesis in human bone cells in vitro. J Pineal Res 1999;27:106-10. https://doi.org/10.1111/j.1600-079X.1999.tb00603.x
  142. Satomura K, Tobiume S, Tokuyama R, et al. Melatonin at pharmacological doses enhances human osteoblastic differentiation in vitro and promotes mouse cortical bone formation in vivo. J Pineal Res 2007;42:231-9. https://doi.org/10.1111/j.1600-079X.2006.00410.x
  143. Roth JA, Kim BG, Lin WL, Cho MI. Melatonin promotes osteoblast differentiation and bone formation. J Biol Chem 1999;274:22041-7. https://doi.org/10.1074/jbc.274.31.22041
  144. Feskanich D, Hankinson SE, Schernhammer ES. Nightshift work and fracture risk: the Nurses' Health Study. Osteoporos Int 2009;20:537-42. https://doi.org/10.1007/s00198-008-0729-5
  145. Reiter RJ, Tan DX, Korkmaz A. The circadian melatonin rhythm and its modulation: possible impact on hypertension. J Hypertens Suppl 2009;27:S17-20. https://doi.org/10.1097/01.hjh.0000358832.41181.bf
  146. Golan D, Halhal B, Glass-Marmor L, et al. Vitamin D supplementation for patients with multiple sclerosis treated with interferon-beta: a randomized controlled trial assessing the effect on flu-like symptoms and immunomodulatory properties. BMC Neurol 2013;13:60. https://doi.org/10.1186/1471-2377-13-60
  147. Brzezinski A. Melatonin in humans. N Engl J Med 1997;336:186-95. https://doi.org/10.1056/NEJM199701163360306
  148. Hajimohammadi M, Shab-Bidar S, Neyestani TR. Vitamin D and serum leptin: a systematic review and meta-analysis of observational studies and randomized controlled trials. Eur J Clin Nutr 2017;71:1144-53. https://doi.org/10.1038/ejcn.2016.245
  149. Upadhyay J, Farr OM, Mantzoros CS. The role of leptin in regulating bone metabolism. Metabolism 2015;64:105-13. https://doi.org/10.1016/j.metabol.2014.10.021
  150. Qiu Y, Sun X, Qiu X, et al. Decreased circulating leptin level and its association with body and bone mass in girls with adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 2007;32:2703-10. https://doi.org/10.1097/BRS.0b013e31815a59e5
  151. Barrios C, Cortes S, Perez-Encinas C, et al. Anthropometry and body composition profile of girls with nonsurgically treated adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 2011;36:1470-7. https://doi.org/10.1097/BRS.0b013e3181f55083
  152. Takeda S. Leptin and beta-blockers in bone metabolism. Clin Calcium 2004;14:241-7.
  153. Thomas T, Gori F, Khosla S, Jensen MD, Burguera B, Riggs BL. Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology 1999;140:1630-8. https://doi.org/10.1210/endo.140.4.6637
  154. Holloway WR, Collier FM, Aitken CJ, et al. Leptin inhibits osteoclast generation. J Bone Miner Res 2002;17:200-9. https://doi.org/10.1359/jbmr.2002.17.2.200
  155. Matkovic V, Ilich JZ, Skugor M, et al. Leptin is inversely related to age at menarche in human females. J Clin Endocrinol Metab 1997;82:3239-45.
  156. Gibson WT, Farooqi IS, Moreau M, et al. Congenital leptin deficiency due to homozygosity for the Delta133G mutation: report of another case and evaluation of response to four years of leptin therapy. J Clin Endocrinol Metab 2004;89:4821-6. https://doi.org/10.1210/jc.2004-0376
  157. Giudici KV PhD, Fisberg RM, Marchioni DML, Peters BSE, Martini LA. Crosstalk between bone and fat tissue: associations between vitamin D, osteocalcin, adipokines, and markers of glucose metabolism among adolescents. J Am Coll Nutr 2017;36:273-80. https://doi.org/10.1080/07315724.2016.1274923
  158. Menendez C, Lage M, Peino R, et al. Retinoic acid and vitamin D(3) powerfully inhibit in vitro leptin secretion by human adipose tissue. J Endocrinol 2001;170:425-31. https://doi.org/10.1677/joe.0.1700425
  159. Kim JH, Choi JH. Pathophysiology and clinical characteristics of hypothalamic obesity in children and adolescents. Ann Pediatr Endocrinol Metab 2013;18:161-7. https://doi.org/10.6065/apem.2013.18.4.161
  160. Maetani M, Maskarinec G, Franke AA, Cooney RV. Association of leptin, 25-hydroxyvitamin D, and parathyroid hormone in women. Nutr Cancer 2009;61:225-31. https://doi.org/10.1080/01635580802455149
  161. Burwell RG, Dangerfield PH, Moulton A, Grivas TB. Adolescent idiopathic scoliosis (AIS), environment, exposome and epigenetics: a molecular perspective of postnatal normal spinal growth and the etiopathogenesis of AIS with consideration of a network approach and possible implications for medical therapy. Scoliosis 2011;6:26. https://doi.org/10.1186/1748-7161-6-26
  162. Wajchenberg M, Martins DE, Lazar M. What is the best way to determine the cause of adolescent idiopathic scoliosis? Ann Transl Med 2015;3:48.
  163. Artaza JN, Norris KC. Vitamin D reduces the expression of collagen and key profibrotic factors by inducing an antifibrotic phenotype in mesenchymal multipotent cells. J Endocrinol 2009;200:207-21.
  164. Lebel A, Lebel VA. Severe progressive scoliosis in an adult female possibly secondary thoracic surgery in childhood treated with scoliosis specific Schroth physiotherapy: case presentation. Scoliosis Spinal Disord 2016;11(Suppl 2):41. https://doi.org/10.1186/s13013-016-0098-3
  165. Brooks WJ, Krupinski EA, Hawes MC. Reversal of childhood idiopathic scoliosis in an adult, without surgery: a case report and literature review. Scoliosis 2009;4:27. https://doi.org/10.1186/1748-7161-4-27
  166. Guillemant J, Le HT, Maria A, Allemandou A, Peres G, Guillemant S. Wintertime vitamin D deficiency in male adolescents: effect on parathyroid function and response to vitamin D3 supplements. Osteoporos Int 2001;12:875-9. https://doi.org/10.1007/s001980170040
  167. Sullivan SS, Rosen CJ, Halteman WA, Chen TC, Holick MF. Adolescent girls in Maine are at risk for vitamin D insufficiency. J Am Diet Assoc 2005;105:971-4. https://doi.org/10.1016/j.jada.2005.03.002
  168. Rockell JE, Green TJ, Skeaff CM, et al. Season and ethnicity are determinants of serum 25-hydroxyvitamin D concentrations in New Zealand children aged 5-14 y. J Nutr 2005;135:2602-8. https://doi.org/10.1093/jn/135.11.2602
  169. Kalkwarf HJ, Khoury JC, Bean J, Elliot JG. Vitamin K, bone turnover, and bone mass in girls. Am J Clin Nutr 2004;80:1075-80. https://doi.org/10.1093/ajcn/80.4.1075
  170. Van Summeren M, Braam L, Noirt F, Kuis W, Vermeer C. Pronounced elevation of undercarboxylated osteocalcin in healthy children. Pediatr Res 2007;61:366-70. https://doi.org/10.1203/pdr.0b013e318030d0b1
  171. Chinda D, Shimoyama T, Iino C, Matsuzaka M, Nakaji S, Fukuda S. Decrease of estradiol and several lifestyle factors, but not helicobacter pylori infection, are significant risks for osteopenia in Japanese females. Digestion 2017;96:103-9. https://doi.org/10.1159/000479317
  172. Xiong B, Sevastik JA, Hedlund R, Sevastik B. Radiographic changes at the coronal plane in early scoliosis. Spine (Phila Pa 1976) 1994;19:159-64. https://doi.org/10.1097/00007632-199401001-00008
  173. Scherrer SA, Begon M, Leardini A, Coillard C, Rivard CH, Allard P. Three-dimensional vertebral wedging in mild and moderate adolescent idiopathic scoliosis. PLoS One 2013;8:e71504. https://doi.org/10.1371/journal.pone.0071504
  174. Begon M, Scherrer SA, Coillard C, Rivard CH, Allard P. Three-dimensional vertebral wedging and pelvic asymmetries in the early stages of adolescent idiopathic scoliosis. Spine J 2015;15:477-86. https://doi.org/10.1016/j.spinee.2014.10.004
  175. Stokes IA, Aronsson DD. Disc and vertebral wedging in patients with progressive scoliosis. J Spinal Disord 2001;14:317-22. https://doi.org/10.1097/00002517-200108000-00006
  176. Modi HN, Suh SW, Song HR, Yang JH, Kim HJ, Modi CH. Differential wedging of vertebral body and intervertebral disc in thoracic and lumbar spine in adolescent idiopathic scoliosis: a cross sectional study in 150 patients. Scoliosis 2008;3:11. https://doi.org/10.1186/1748-7161-3-11
  177. Will RE, Stokes IA, Qiu X, Walker MR, Sanders JO. Cobb angle progression in adolescent scoliosis begins at the intervertebral disc. Spine (Phila Pa 1976) 2009;34:2782-6. https://doi.org/10.1097/BRS.0b013e3181c11853
  178. Taylor TK, Ghosh P, Bushell GR. The contribution of the intervertebral disk to the scoliotic deformity. Clin Orthop Relat Res 1981;(156):79-90.
  179. Keenan BE, Izatt MT, Askin GN, et al. Sequential magnetic resonance imaging reveals individual level deformities of vertebrae and discs in the growing scoliotic spine. Spine Deform 2017;5:197-207. https://doi.org/10.1016/j.jspd.2016.10.002
  180. Wang S, Qiu Y, Ma W, et al. Comparison of disc and vertebral wedging between patients with adolescent idiopathic scoliosis and Chiari malformation-associated scoliosis. J Spinal Disord Tech 2012;25:277-84. https://doi.org/10.1097/BSD.0b013e31821f4f10
  181. Stokes IA. Mechanical modulation of spinal growth and progression of adolescent scoliosis. Stud Health Technol Inform 2008;135:75-83.
  182. Stokes IA. Analysis and simulation of progressive adolescent scoliosis by biomechanical growth modulation. Eur Spine J 2007;16:1621-8. https://doi.org/10.1007/s00586-007-0442-7
  183. Pollintine P, Luo J, Offa-Jones B, Dolan P, Adams MA. Bone creep can cause progressive vertebral deformity. Bone 2009;45:466-72. https://doi.org/10.1016/j.bone.2009.05.015
  184. Luo J, Pollintine P, Gomm E, Dolan P, Adams MA. Vertebral deformity arising from an accelerated “creep” mechanism. Eur Spine J 2012;21:1684-91. https://doi.org/10.1007/s00586-012-2279-y
  185. Wren TA, Ponrartana S, Aggabao PC, Poorghasamians E, Gilsanz V. Association between vertebral cross-sectional area and vertebral wedging in children and adolescents: a cross-sectional analysis. J Bone Miner Res 2017;32:2257-62. https://doi.org/10.1002/jbmr.3210
  186. Wang WJ, Sun C, Liu Z, et al. Transcription factor Runx2 in the low bone mineral density of girls with adolescent idiopathic scoliosis. Orthop Surg 2014;6:8-14. https://doi.org/10.1111/os.12087
  187. Obarzanek E, Hunsberger SA, Van Horn L, et al. Safety of a fat-reduced diet: the Dietary Intervention Study in Children (DISC). Pediatrics 1997;100:51-9. https://doi.org/10.1542/peds.100.1.51
  188. Obarzanek E, Hunsberger SA, van Horn L, et al. Safety of a fat-reduced diet: the Dietary Intervention Study in Children (DISC). Pediatrics 1997;100:51-9. https://doi.org/10.1542/peds.100.1.51

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