Are volumetric bone mineral density and bone micro-architecture associated with leptin and soluble leptin receptor levels in adolescent idiopathic scoliosis? - A case-control study

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Tam, Elisa M S ^a   Yu, Fiona W P ^a   Hung, Vivian W Y ^a   Liu, Zhen ^a,b   Liu, King Lok ^a   Ng, Bobby K W ^a   Lee, Simon K M ^a   Qiu, Yong ^a,b   Cheng, Jack C Y ^a   Lam, Tsz Ping ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTIN; LEPTIN RECEPTOR;

ADOLESCENT; ADOLESCENT IDIOPATHIC SCOLIOSIS; ADULT; AGED; ARTICLE; BODY HEIGHT; BODY WEIGHT; BONE DENSITY; BONE METABOLISM; CASE CONTROL STUDY; CHILD; CHINESE; CONTROLLED STUDY; CORTICAL BONE; DISEASE ASSOCIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HIGH RESOLUTION COMPUTER TOMOGRAPHY; HUMAN; MAJOR CLINICAL STUDY; MALE; MORPHOMETRICS; PERIMETER; PROTEIN BLOOD LEVEL; RADIUS; TRABECULAR BONE; VERY ELDERLY; VOLUMETRY; ANTHROPOMETRY; BLOOD; BODY MASS; BONE; COMPUTER ASSISTED TOMOGRAPHY; PATHOLOGY; PATHOPHYSIOLOGY; RADIOGRAPHY; SCOLIOSIS; SOLUBILITY; THREE DIMENSIONAL IMAGING;

ADOLESCENT; ANTHROPOMETRY; BODY MASS INDEX; BONE AND BONES; BONE DENSITY; CASE-CONTROL STUDIES; CHILD; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; LEPTIN; RECEPTORS, LEPTIN; SCOLIOSIS; SOLUBILITY; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84895521870     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087939     Document Type: Article

References (90)

1. Weinstein SL, Dolan LA, Cheng JC, Danielsson A, Morcuende JA (2008) Adolescent idiopathic scoliosis. Lancet 371: 1527-1537. (Pubitemid 351626190)
2. Luk K, Lee C, Cheung K, Cheng J, Ng B, et al. (2010) Clinical Effectiveness of School Screening for Adolescent Idiopathic Scoliosis: A Large Population-Based Retrospective Cohort Study. Spine 35: 1607-1614.
3. Cheung CSK, Lee WTK, Tse YK, Tang SP, Lee KM, et al. (2003) Abnormal Peri-pubertal Anthropometric Measurements and Growth Pattern in Adolescent Idiopathic Scoliosis - a Study of 598 Patients. Spine 28: 2152-2157. (Pubitemid 37140206)
4. Cheng JCY, Qin L, Cheung CSK, Sher AHL, Lee KM, et al. (2000) Generalized Low Areal and Volumetric Bone Mineral Density in Adolescent Idiopathic Scoliosis. Journal of Bone and Mineral Research 15: 1587-1595. (Pubitemid 30484529)
5. Wang WJ, Hung VW, Lam TP, Ng BK, Qin L, et al. (2010) The association of disproportionate skeletal growth and abnormal radius dimension ratio with curve severity in adolescent idiopathic scoliosis. European Spine Journal.
6. Cheung CSK, Lee WTK, Tse YK, Guo X, Qin L, et al. (2006) Generalized osteopenia in Adolescent Idiopathic Scoliosis - Association with abnormal pubertal growth, bone turnover, and calcium intake? Spine 31: 330-338. (Pubitemid 43214775)
7. Cheng JCY, Guo X (1997) Osteoporosis in Adolescent Idiopathic Scoliosis - A Primary Problem or Secondary to the Spinal Deformity? Spine 22: 1716-1721. (Pubitemid 28076403)
8. Archer IA, Dickson RA (1985) Stature and idiopathic scoliosis. A prospective study. J Bone Joint Surg Br 67: 185-188. (Pubitemid 15109865)
9. Cheng JCY, Guo X, Sher AH (1999) Persistent osteopenia in adolescent idiopathic scoliosis. A longitudinal follow up study. Spine (Phila Pa 1976) 24: 1218-1222.
10. Buric M, Momcilovic B (1982) Growth pattern and skeletal age in school girls with idiopathic scoliosis. Clin Orthop Relat Res: 238-242. (Pubitemid 12034346)
11. Cook SD, Harding AF, Morgan EL, Nicholson RJ, Thomas KA, et al. (1987) Trabecular bone mineral density in idiopathic scoliosis. J Pediatr Orthop 7: 168-174. (Pubitemid 17032066)
12. Nordwall A, Willner S (1975) A study of skeletal age and height in girls with idiopathic scoliosis. Clin Orthop Relat Res: 6-10.
13. Willner S (1974) A study of growth in girls with adolescent idiopathic structural scoliosis. Clin Orthop Relat Res: 129-135.
14. Willner S (1974) Growth in height of children with scoliosis. Acta Orthop Scand 45: 854-866.
15. Liu Z, Tam EMS, Sun GQ, Lam TP, Zhu ZZ, et al. (2012) Abnormal Leptin Bioavailability in Adolescent Idiopathic Scoliosis - an Important New Finding. Spine (Phila Pa 1976) 37: 599-604.
16. Hung VWY, Qin L, Cheung CSK, Lam TP, Ng BKW, et al. (2005) Osteopenia: a new prognostic factor of curve progression in adolescent idiopathic scoliosis. THe Journal of Bone and Joint Surgery 87: 2709-2716. (Pubitemid 41747037)
17. Beltowski J (2012) Leptin and the regulation of endothelial function in physiological and pathological conditions. Clin Exp Pharmacol Physiol 39: 168-178.
18. Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, et al. (1995) Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269: 540-543.
19. Dardeno TA, Chou SH, Moon HS, Chamberland JP, Fiorenza CG, et al. (2010) Leptin in human physiology and therapeutics. Front Neuroendocrinol 31: 377-393.
20. Mantzoros CS, Magkos F, Brinkoetter M, Sienkiewicz E, Dardeno TA, et al. (2011) Leptin in human physiology and pathophysiology. Am J Physiol Endocrinol Metab 301: E567-584.
21. Kelesidis T, Kelesidis I, Chou S, Mantzoros CS (2010) Narrative review: the role of leptin in human physiology: emerging clinical applications. Ann Intern Med 152: 93-100.
22. Fruhbeck G (2006) Intracellular signalling pathways activated by leptin. Biochem J 393: 7-20.
23. Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, et al. (1995) Weight-reducing effects of the plasma protein encoded by the obese gene. Science 269: 543-546.
24. Tartaglia LA, Dembski M, Weng X, Deng N, Culpepper J, et al. (1995) Identification and expression cloning of a leptin receptor, OB-R. Cell 83: 1263-1271. (Pubitemid 26007816)
25. Lee GH, Proenca R, Montez JM, Carroll KM, Darvishzadeh JG, et al. (1996) Abnormal splicing of the leptin receptor in diabetic mice. Nature 379: 632-635. (Pubitemid 26053452)
26. Cioffi JA, Shafer AW, Zupancic TJ, Smith-Gbur J, Mikhail A, et al. (1996) Novel B219/OB receptor isoforms: possible role of leptin in hematopoiesis and reproduction. Nat Med 2: 585-589. (Pubitemid 26151519)
27. Bennett BD, Solar GP, Yuan JQ, Mathias J, Thomas GR, et al. (1996) A role for leptin and its cognate receptor in hematopoiesis. Curr Biol 6: 1170-1180. (Pubitemid 26368751)
28. Hess R, Pino AM, Rios S, Fernandez M, Rodriguez JP (2005) High affinity leptin receptors are present in human mesenchymal stem cells (MSCs) derived from control and osteoporotic donors. J Cell Biochem 94: 50-57. (Pubitemid 41420323)
29. Reseland JE, Syversen U, Bakke I, Qvigstad G, Eide LG, et al. (2001) Leptin is expressed in and secreted from primary cultures of human osteoblasts and promotes bone mineralization. J Bone Miner Res 16: 1426-1433. (Pubitemid 32675194)
30. Zhang F, Chen Y, Heiman M, Dimarchi R (2005) Leptin: structure, function and biology. Vitam Horm 71: 345-372. (Pubitemid 43589034)
31. Steppan CM, Crawford DT, Chidsey-Frink KL, Ke H, Swick AG (2000) Leptin is a potent stimulator of bone growth in ob/ob mice. Regul Pept 92: 73-78.
32. Gordeladze JO, Drevon CA, Syversen U, Reseland JE (2002) Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: Impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem 85: 825-836. (Pubitemid 34462792)
33. Maor G, Rochwerger M, Segev Y, Phillip M (2002) Leptin acts as a growth factor on the chondrocytes of skeletal growth centers. J Bone Miner Res 17: 1034-1043. (Pubitemid 34535141)
34. Thomas T, Gori F, Khosla S, Jensen MD, Burguera B, et al. (1999) Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology 140: 1630-1638. (Pubitemid 29149231)
35. Handschin AE, Trentz OA, Hemmi S, Wedler V, Trentz O, et al. (2007) Leptin increases extracellular matrix mineralization of human osteoblasts from heterotopic ossification and normal bone. Ann Plast Surg 59: 329-333. (Pubitemid 47329719)
36. Lamghari M, Tavares L, Camboa N, Barbosa MA (2006) Leptin effect on RANKL and OPG expression in MC3T3-E1 osteoblasts. J Cell Biochem 98: 1123-1129. (Pubitemid 44128354)
37. Holloway WR, Collier FM, Aitken CJ, Myers DE, Hodge JM, et al. (2002) Leptin inhibits osteoclast generation. J Bone Miner Res 17: 200-209. (Pubitemid 34087652)
38. Elefteriou F, Takeda S, Ebihara K, Magre J, Patano N, et al. (2004) Serum leptin level is a regulator of bone mass. Proceedings of the National Academy of Sciences of the United States of America 101: 3258-3263. (Pubitemid 38327768)
39. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, et al. (2000) Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 100: 197-207. (Pubitemid 30064908)
40. Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, et al. (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111: 305-317. (Pubitemid 35345151)
41. Ducy P, Schinke T, Karsenty G (2000) The osteoblast: a sophisticated fibroblast under central surveillance. Science 289: 1501-1504.
42. Matkovic V, Ilich JZ, Skugor M, Badenhop NE, Goel P, et al. (1997) Leptin is inversely related to age at menarche in human females. J Clin Endocrinol Metab 82: 3239-3245. (Pubitemid 27419064)
43. Quinton ND, Smith RF, Clayton PE, Gill MS, Shalet S, et al. (1999) Leptin binding activity changes with age: the link between leptin and puberty. Journal of Clinical Endocrinology and Metabolism 84: 2336-2341.
44. Grivas TB, Burwell RG, Mihas C, Vasiliadis ES, Triantafyllopoulos G, et al. (2009) Relatively lower body mass index is associated with an excess of severe truncal asymmetry in healthy adolescents: Do white adipose tissue, leptin, hypothalamus and sympathetic nervous system influence truncal growth asymmetry? Scoliosis 4: 13.
45. Wu T, Sun X, Zhu Z, Zheng X, Qian B, et al. (2012) Role of high central leptin activity in a scoliosis model created in bipedal amputated mice. Stud Health Technol Inform 176: 31-35.
46. Qiu Y, Sun X, Qiu X, Li W, Zhu Z, et al. (2007) Decreased circulating leptin level and its association with body and bone mass in girls with adolescent idiopathic scoliosis. Spine (Phila Pa 1976) 32: 2703-2710.
47. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, et al. (1996) Serum immunoreactive-leptin concentrations in normal-weight and obese humans. New England Journal of Medicine 334: 292-295. (Pubitemid 26033933)
48. Hassink SG, Sheslow DV, de Lancey E, Opentanova I, Considine RV, et al. (1996) Serum leptin in children with obesity: relationship to gender and development. Pediatrics 98: 201-203. (Pubitemid 26262130)
49. Lenke LG, Betz RR, Harms J, Bridwell KH, Clements DH, et al. (2001) Adolescent idiopathic scoliosis. A new classification to determine extent of spinal arthrodesis. Journal of Bone and Joint Surgery - Series A 83: 1169-1181. (Pubitemid 32735067)
50. Kono K, Asazuma T, Suzuki N, Ono T (2000) Body height correction in scoliosis patients for pulmonary function test. J Orthop Surg (Hong Kong) 8: 19-26. (Pubitemid 32963041)
51. Ylikoski M (2003) Height of girls with adolescent idiopathic scoliosis. European Spine Journal 12: 288-291.
52. Cheng JCY, Leung SSF, Lau J (1996) Anthropometric Measurements and Body Proportions Among Chinese Children. Clinical Orthopaedics and Related Research 323: 22-30. (Pubitemid 26065420)
53. Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, et al. (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24: 1033-1042.
54. Liu XS, Cohen A, Shane E, Yin PT, Stein EM, et al. (2010) Bone density, geometry, microstructure, and stiffness: Relationships between peripheral and central skeletal sites assessed by DXA, HR-pQCT, and cQCT in premenopausal women. J Bone Miner Res 25: 2229-2238.
55. Laib A, Hauselmann HJ, Ruegsegger P (1998) In vivo high resolution 3D-QCT of the human forearm. Technol Health Care 6: 329-337. (Pubitemid 29090456)
56. MacNeil JA, Boyd SK (2007) Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys 29: 1096-1105. (Pubitemid 350052626)
57. Laib A, Hildebrand T, Hauselmann HJ, Ruegsegger P (1997) Ridge number density: a new parameter for in vivo bone structure analysis. Bone 21: 541-546. (Pubitemid 28029698)
58. Hildebrand T, Rüegsegger P (1997) A new method for the model-independent assessment of thickness in three-dimensional images. Journal of Microscopy 185: 67-75. (Pubitemid 27060526)
59. Laib A, Ruegsegger P (1999) Calibration of trabecular bone structure measurements of in vivo three-dimensional peripheral quantitative computed tomography with 28-microm-resolution microcomputed tomography. Bone 24: 35-39. (Pubitemid 28546704)
60. Huang L, Wang Z, Li C (2001) Modulation of circulating leptin levels by its soluble receptor. J Biol Chem 276: 6343-6349.
61. Chan JL, Bluher S, Yiannakouris N, Suchard MA, Kratzsch J, et al. (2002) Regulation of circulating soluble leptin receptor levels by gender, adiposity, sex steroids, and leptin: observational and interventional studies in humans. Diabetes 51: 2105-2112. (Pubitemid 34729014)
62. Lou PH, Yang G, Huang L, Cui Y, Pourbahrami T, et al. (2010) Reduced body weight and increased energy expenditure in transgenic mice over-expressing soluble leptin receptor. PLoS One.
63. Zhang J, Scarpace PJ (2009) The soluble leptin receptor neutralizes leptin-mediated STAT3 signalling and anorexic responses in vivo. Br J Pharmacol 158: 475-482.
64. Gavrilova O, Barr V, Marcus-Samuels B, Reitman M (1997) Hyperleptinemia of pregnancy associated with the appearance of a circulating form of the leptin receptor. Journal of Biological Chemistry 272: 30546-30551. (Pubitemid 27512268)
65. Yang G, Ge H, Boucher A, Yu X, Li C (2004) Modulation of direct leptin signaling by soluble leptin receptor. Mol Endocrinol 18: 1354-1362. (Pubitemid 38692175)
66. Zastrow O, Seidel B, Kiess W, Thiery J, Keller E, et al. (2003) The soluble leptin receptor is crucial for leptin action: evidence from clinical and experimental data. Int J Obes Relat Metab Disord 27: 1472-1478. (Pubitemid 38019159)
67. Tu H, Kastin AJ, Hsuchou H, Pan W (2008) Soluble receptor inhibits leptin transport. J Cell Physiol 214: 301-305. (Pubitemid 350308985)
68. Yannakoulia M, Yiannakouris N, Bluher S, Matalas AL, Klimis-Zacas D, et al. (2003) Body fat mass and macronutrient intake in relation to circulating soluble leptin receptor, free leptin index, adiponectin, and resistin concentrations in healthy humans. J Clin Endocrinol Metab 88: 1730-1736. (Pubitemid 36623396)
69. Misra M, Miller KK, Almazan C, Ramaswamy K, Aggarwal A, et al. (2004) Hormonal and body composition predictors of soluble leptin receptor, leptin, and free leptin index in adolescent girls with anorexia nervosa and controls and relation to insulin sensitivity. J Clin Endocrinol Metab 89: 3486-3495. (Pubitemid 38951925)
70. Mann DR, Johnson AO, Gimpel T, Castracane VD (2003) Changes in circulating leptin, leptin receptor, and gonadal hormones from infancy until advanced age in humans. J Clin Endocrinol Metab 88: 3339-3345. (Pubitemid 36877514)
71. Malincikova J, Stejskal D, Hrebicek J (2000) Serum leptin and leptin receptors in healthy prepubertal children: relations to insulin resistance and lipid parameters, body mass index (BMI), tumor necrosis factor alpha (TNF alpha), heart fatty acid binding protein (hFABP), and IgG anticardiolipin (ACL-IgG). Acta Univ Palacki Olomuc Fac Med 143: 51-57.
72. Celi F, Galmacci G, Bini V, Papi F, Contessa G, et al. (2005) BMI-conditional standard of leptin serum values in children: proposal of a statistical procedure for the analysis of influencing variables. J Pediatr Endocrinol Metab 18: 1399-1408. (Pubitemid 43109377)
73. Kratzsch J, Lammert A, Bottner A, Seidel B, Mueller G, et al. (2002) Circulating soluble leptin receptor and free leptin index during childhood, puberty, and adolescence. Journal of Clinical Endocrinology and Metabolism 87: 4587-4594. (Pubitemid 35247045)
74. Schaab M, Kausch H, Klammt J, Nowicki M, Anderegg U, et al. (2012) Novel regulatory mechanisms for generation of the soluble leptin receptor: implications for leptin action. PLoS One 7: e34787.
75. Cheng JC, Hung VW, Lee WT, Yeung HY, Lam TP, et al. (2006) Persistent osteopenia in adolescent idiopathic scoliosis - longitudinal monitoring of bone mineral density until skeletal maturity. Stud Health Technol Inform 123: 47-51.
76. Yeung HY, Qin L, Hung VW, Lee KM, Guo X, et al. (2006) Lower degree of mineralization found in cortical bone of adolescent idiopathic scoliosis (AIS). Stud Health Technol Inform 123: 599-604.
77. Snyder BD, Katz DA, Myers ER, Breitenbach MA, Emans JB (2005) Bone density accumulation is not affected by brace treatment of idiopathic scoliosis in adolescent girls. J Pediatr Orthop 25: 423-428. (Pubitemid 40884953)
78. Lee WTK, Cheung CSK, Tse YK, Guo X, Qin L, et al. (2005) Generalized low bone mass of girls with adolescent idiopathic scoliosis is related to inadequate calcium intake and weight bearing physical activity in peripubertal period. Osteoporos Int 16: 1024-1035. (Pubitemid 41225088)
79. Lam TP, Hung VW, Yeung HY, Tse YK, Chu WC, et al. (2011) Abnormal bone quality in adolescent idiopathic scoliosis: a case-control study on 635 subjects and 269 normal controls with bone densitometry and quantitative ultrasound. Spine (Phila Pa 1976) 36: 1211-1217.
80. Li XF, Li H, Liu ZD, Dai LY (2008) Low bone mineral status in adolescent idiopathic scoliosis. Eur Spine J 17: 1431-1440.
81. Velis KP, Healey JH, Schneider R (1989) Peak skeletal mass assessment in young adults with idiopathic scoliosis. Spine (Phila Pa 1976) 14: 706-711.
82. Saggese G, Baroncelli GI, Bertelloni S (2001) Osteoporosis in children and adolescents: diagnosis, risk factors, and prevention. J Pediatr Endocrinol Metab 14: 833-859. (Pubitemid 32737355)
83. Dempster DW (1992) Bone Remodeling. In: Coe FL, Favus MJ, editors. Disorders of bone and mineral metabolism. New York: Raven Press. 355-380.
84. Hamrick MW, Della-Fera MA, Choi YH, Pennington C, Hartzell D, et al. (2005) Leptin treatment induces loss of bone marrow adipocytes and increases bone formation in leptin-deficient ob/ob mice. J Bone Miner Res 20: 994-1001. (Pubitemid 40712824)
85. Lorentzon R, Alehagen U, Boquist L (1986) Osteopenia in mice with genetic diabetes. Diabetes Res Clin Pract 2: 157-163. (Pubitemid 17231071)
86. Thomas T (2003) Leptin: a potential mediator for protective effects of fat mass on bone tissue. Joint Bone Spine 70: 18-21.
87. Baldock PA, Allison S, McDonald MM, Sainsbury A, Enriquez RF, et al. (2006) Hypothalamic regulation of cortical bone mass: opposing activity of Y2 receptor and leptin pathways. J Bone Miner Res 21: 1600-1607. (Pubitemid 44484605)
88. Wren AM, Small CJ, Abbott CR, Jethwa PH, Kennedy AR, et al. (2002) Hypothalamic actions of neuromedin U. Endocrinology 143: 4227-4234. (Pubitemid 35239552)
89. Sato S, Hanada R, Kimura A, Abe T, Matsumoto T, et al. (2007) Central control of bone remodeling by neuromedin U. Nat Med 13: 1234-1240. (Pubitemid 47530632)
90. Hamrick MW, Pennington C, Newton D, Xie D, Isales C (2004) Leptin deficiency produces contrasting phenotypes in bones of the limb and spine. Bone 34: 376-383. (Pubitemid 38314902)