Pubertal Disorders and Bone Maturation

Endocrinology and Metabolism Clinics of North America

Volumn 41, Issue 4, 2012, Pages 805-825

  Lazar, Liora ^a,b   Phillip, Moshe ^a,b  

^a SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Bone age; Delayed puberty; Normal puberty; Precocious puberty; Pubertal growth spurt; Skeletal maturation

Indexed keywords

ANASTROZOLE; AROMATASE INHIBITOR; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GONADORELIN DERIVATIVE; GROWTH HORMONE; LEPTIN RECEPTOR; LETROZOLE; SEX HORMONE; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; TESTOSTERONE;

ADRENARCHE; AGE DETERMINATION; BODY HEIGHT; BONE AGE; BONE GROWTH; BONE MATURATION; DELAYED PUBERTY; DIAGNOSTIC VALUE; DRUG EFFICACY; DRUG MEGADOSE; EPIPHYSIS PLATE; GONADORELIN TEST; GROWTH DISORDER; HUMAN; PRECOCIOUS PUBERTY; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; PUBERTY DISORDERS; RELIABILITY; REVIEW; SEXUAL MATURATION; SHORT STATURE; SIGNAL TRANSDUCTION; TALL STATURE;

ADOLESCENT; ADOLESCENT DEVELOPMENT; AGE DETERMINATION BY SKELETON; BODY HEIGHT; BONE DEVELOPMENT; CHILD; CHILD DEVELOPMENT; EPIPHYSES; FEMALE; GONADOTROPIN-RELEASING HORMONE; GROWTH DISORDERS; GROWTH HORMONE; HUMANS; MALE; PUBERTY; PUBERTY, DELAYED; PUBERTY, PRECOCIOUS;

EID: 84867942713     PISSN: 08898529     EISSN: 15584410     Source Type: Journal    
DOI: 10.1016/j.ecl.2012.08.003     Document Type: Review

References (96)

1. Grumbach M.M., Styne D.M. Puberty: ontogeny, neuroendocrinology, physiology and disorders. Williams' textbook of endocrinology 2011, 1055-1201. W.B. Saunders Co, Philadelphia. 12th edition. S. Melmed, K.S. Polonsky, P.R. Larsen (Eds.).
2. Marshall W.A., Tanner J.M. Variations in the pattern of pubertal changes in girls. Arch Dis Child 1969, 44(235):291-303.
3. Marshall W.A., Tanner J.M. Variations in the pattern of pubertal changes in boys. Arch Dis Child 1970, 45(239):13-23.
4. Tanner J.M., Whitehouse R.H., Marubini E., et al. The adolescent growth spurt of boys and girls of the Harpenden growth study. Ann Hum Biol 1976, 3(2):109-126.
5. Palmert M.R., Boepple P.A. Variation in the timing of puberty: clinical spectrum and genetic investigation. J Clin Endocrinol Metab 2001, 86(6):2364-2368.
6. Parent A.S., Teilmann G., Juul A., et al. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 2003, 24(5):668-693.
7. Hochberg Z. Endocrine control of skeletal maturation 2002, Karger, Basel (Switzerland).
8. Brauner R., Adan L., Malandry A., et al. Adult height in girls with idiopathic true precocious puberty. J Clin Endocrinol Metab 1994, 79(2):415-420.
9. Speiser P.W., White P.C. Congenital adrenal hyperplasia. N Engl J Med 2003, 349(8):776-788.
10. New M.I. Extensive clinical experience: nonclassical 21-hydroxylase deficiency. J Clin Endocrinol Metab 2006, 91(11):4205-4214.
11. Schlesinger S., MacGillivray M.H., Munschauer R.W. Acceleration of growth and bone maturation in childhood thyrotoxicosis. J Pediatr 1973, 83(2):233-236.
12. Ibañez L., Virdis R., Potau N., et al. Natural history of premature pubarche: an auxological study. J Clin Endocrinol Metab 1992, 74(2):254-257.
13. Volta C., Bernasconi S., Cisternino M., et al. Isolated premature thelarche and thelarche variant: clinical and auxological follow-up of 119 girls. J Endocrinol Invest 1998, 21(3):180-183.
14. Russell D.L., Keil M.F., Bonat S.H., et al. The relation between skeletal maturation and adiposity in African American and Caucasian children. J Pediatr 2001, 139(6):844-848.
15. Dickerman Z., Loewinger J., Laron Z. The pattern of growth in children with constitutional tall stature from birth to age 9 years. A longitudinal study. Acta Paediatr Scand 1984, 73(4):530-536.
16. Clark R.N. Congenital dysplasias and dwarfism. Pediatr Rev 1990, 12(5):149-159.
17. Kulin H.E., Bwibo N., Mutie D., et al. The effect of chronic childhood malnutrition on pubertal growth and development. Am J Clin Nutr 1982, 36(3):527-536.
18. Alvear J., Artaza C., Vial M., et al. Physical growth and bone age of survivors of protein energy malnutrition. Arch Dis Child 1986, 61(3):257-262.
19. Pantsiouou S., Stanhope R., Uruena M., et al. Growth prognosis and growth after menarche in primary hypothyroidism. Arch Dis Child 1991, 66(7):838-840.
20. Sedlmeyer I.L., Palmert M.R. Delayed puberty: analysis of a large case series from an academic center. J Clin Endocrinol Metab 2002, 87(4):1613-1620.
21. Tanner J.M., Whitehouse R.H. A note on the bone age at which patients with true isolated growth hormone deficiency enter puberty. J Clin Endocrinol Metab 1975, 41(4):788-790.
22. Martin D.D., Wit J.M., Hochberg Z., et al. The use of bone age in clinical practice-part 1 & part 2. Horm Res Paediatr 2011, 76(1):1-16.
23. Greulich W., Pyle S. Radiographic atlas of the skeletal development of the hand and wrist 1959, Stanford University Press, Stanford (CA). 2nd edition.
24. Tanner J.M., Whitehouse R.H., Marshall W.A., et al. Assessment of skeletal maturity and prediction of adult height (TW2 method) 1975, Academic Press, London.
25. Tanner J.M., Landt K.W., Cameron N., et al. Prediction of adult height from height and bone age in childhood. A new system of equations (TW Mark II) based on a sample including very tall and very short children. Arch Dis Child 1983, 58(10):767-776.
26. Tanner J.M., Healy M., Goldstein H., et al. Assessment of skeletal maturity and prediction of adult height (TW3 method) 2001, WB Saunders, London. 3rd edition.
27. Thodberg H.H. Clinical review: an automated method for determination of bone age. J Clin Endocrinol Metab 2009, 94(7):2239-2244.
28. Bayley N., Pinneau S.R. Tables for predicting adult height from skeletal age: revised for use with the Greulich-Pyle hand standards. J Pediatr 1952, 40(4):423-441.
29. Roche A.F., Wainer H., Thissen D. The RWT method for the prediction of adult stature. Pediatrics 1975, 56(6):1027-1033.
30. Thodberg H.H., Neuhof J., Ranke M.B., et al. Validation of bone age methods by their ability to predict adult height. Horm Res Paediatr 2010, 74(1):15-22.
31. Nilsson O., Marino R., De Luca F., et al. Endocrine regulation of the growth plate. Horm Res 2005, 64(4):157-165.
32. Veldhuis J.D., Metzger D.L., Martha P.M., et al. Estrogen and testosterone, but not a nonaromatizable androgen, direct network integration of hypothalamo-somatotrope (Growth Hormone)-insulin-like growth factor I axis in the human: evidence from pubertal pathophysiology and sex-steroid replacement. J Clin Endocrinol Metab 1997, 82(10):3414-3420.
33. Luna A., Wilson D., Wibbelsman C., et al. Somatomedins in adolescence; a cross sectional study of the effect of puberty on plasma insulin-like growth factor I and II levels. J Clin Endocrinol Metab 1983, 57(2):268-271.
34. Isaksson O.G., Lindahl A., Nilsson A., et al. Mechanism of the stimulatory effect of growth hormone on longitudinal bone growth. Endocr Rev 1987, 8(4):426-438.
35. Weise M., De-Levi S., Barnes K.M., et al. Effects of estrogen on growth plate senescence and epiphyseal fusion. Proc Natl Acad Sci U S A 2001, 98(12):6871-6876.
36. Phillip M., Maor G., Assa S., et al. Testosterone stimulates growth of tibial epiphyseal growth plate and insulin-like growth factor-I-receptor abundance and growth in hypophysectomized and castrated rats. Endocrine 2001, 16(1):1-6.
37. Maor G., Rochberger M., Segev Y., et al. Leptin acts as a growth factor on the chondrocytes of skeletal growth center. J Bone Miner Res 2002, 17(6):1034-1043.
38. Morishima A., Grumbach M.M., Simpson E.R., et al. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J Clin Endocrinol Metab 1995, 80(12):3689-3698.
39. Smith E.P., Boyd J., Frank G.R., et al. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 1994, 331(16):1056-1061.
40. Zachmann M., Prader A., Sobel E.H., et al. Indirect evidence for the importance of estrogens in pubertal growth of girls. J Pediatr 1986, 108(5 Pt 1):694-697.
41. Nilsson L.O., Boman A., Sävendahl L., et al. Demonstration of estrogen receptor-β immunoreactivity in human growth plate cartilage. J Clin Endocrinol Metab 1999, 84(1):370-373.
42. Chagin A.S., Sävendahl L. GPR30 estrogen receptor expression in the growth plate declines as puberty progresses. J Clin Endocrinol Metab 2007, 92(12):4873-4877.
43. Weise M., Flor A., Barnes K.M., et al. Determinants of growth during gonadotropin-releasing hormone analog therapy for precocious puberty. J Clin Endocrinol Metab 2004, 89(1):103-107.
44. Buckler J.M. Skeletal age changes in puberty. Arch Dis Child 1984, 59(2):115-119.
45. Ontell F.K., Ivanovic M., Ablin D.S., et al. Bone age in children of diverse ethnicity. AJR Am J Roentgenol 1996, 167(6):1395-1398.
46. Marshall W.A. Interrelationships of skeletal maturation, sexual development and somatic growth in man. Ann Hum Biol 1974, 1(1):29-40.
47. Flor-Cisneros A., Roemmich J.N., Rogol A.D., et al. Bone age and onset of puberty in normal boys. Mol Cell Endocrinol 2006, 25:254-55:202-206.
48. Klein K.O., Larmore K.A., de Lancey E., et al. Effect of obesity on estradiol level, and its relationship to leptin, bone maturation, and bone mineral density in children. J Clin Endocrinol Metab 1998, 83(10):3469-3475.
49. Lazar L., Lebenthal Y., Shalitin S., et al. Natural history of idiopathic advanced bone age diagnosed in childhood: pattern of growth and puberty. Horm Res Paediatr 2011, 75(1):49-55.
50. de Waal W.J., Greyn-Fokker M.H., Stijnen T., et al. Accuracy of final height prediction and effect of growth-reductive therapy in 362 constitutionally tall children. J Clin Endocrinol Metab 1996, 81(3):1206-1216.
51. Carel J.C., Hay F., Coutant R., et al. Gonadotropin-releasing hormone agonist treatment of girls with constitutional short stature and normal pubertal development. J Clin Endocrinol Metab 1996, 81(9):3318-3322.
52. Yanovski J.A., Rose S.R., Municchi G., et al. Treatment with a luteinizing hormone-releasing hormone agonist in adolescents with short stature. N Engl J Med 2003, 348(10):908-917.
53. Lanes R., Gunczler P. Final height after combined growth hormone and gonadotrophin-releasing hormone analogue therapy in short healthy children entering into normally timed puberty. Clin Endocrinol (Oxf) 1998, 49(2):197-202.
54. Pasquino A.M., Pucarelli I., Roggini M., et al. Adult height in short normal girls treated with gonadotropin-releasing hormone analogs and growth hormone. J Clin Endocrinol Metab 2000, 85(2):619-622.
55. van Gool S.A., Kamp G.A., Visser-van Balen H., et al. Final height outcome after three years of growth hormone and gonadotropin-releasing hormone agonist treatment in short adolescents with relatively early puberty. J Clin Endocrinol Metab 2007, 92(4):1402-1408.
56. Hero M., Norjavaara E., Dunkel L. Inhibition of estrogen biosynthesis with a potent aromatase inhibitor increases predicted adult height in boys with idiopathic short stature: a randomized controlled trial. J Clin Endocrinol Metab 2005, 90(12):6396-6402.
57. Hero M., Toiviainen-Salo S., Wickman S., et al. Vertebral morphology in aromatase inhibitor-treated males with idiopathic short stature or constitutional delay of puberty. J Bone Miner Res 2010, 25(7):1536-1543.
58. Drop S.L., De Waal W.J., De Muinck Keizer-Schrama S.M. Sex steroid treatment of constitutionally tall stature. Endocr Rev 1998, 19(5):540-558.
59. Fontoura M., Brauner R., Prevot C., et al. Precocious puberty in girls: early diagnosis of a slowly progressing variant. Arch Dis Child 1989, 64(8):1170-1176.
60. Palmert M.R., Malin H.V., Boepple P.A. Unsustained or slowly progressive puberty in young girls: initial presentation and long-term follow-up of 20 untreated patients. J Clin Endocrinol Metab 1999, 84(2):415-423.
61. Klein K.O. Precocious puberty: who has it? Who should be treated?. J Clin Endocrinol Metab 1999, 84(2):411-414.
62. Lazar L., Pertzelan A., Weintrob N., et al. Sexual precocity in boys: accelerated versus slowly progressive puberty gonadotropin-suppressive therapy and final height. J Clin Endocrinol Metab 2001, 86(9):4127-4132.
63. Kauli R., Galatzer A., Kornreich L., et al. Final height of girls with central precocious puberty, untreated versus treated with cyproterone acetate or GnRH analogue. A comparative study with re-evaluation of predictions by the Bayley-Pinneau method. Horm Res 1997, 47(2):54-61.
64. Brito V.N., Latronico A.C., Cukier P., et al. Factors determining normal adult height in girls with gonadotropin-dependent precocious puberty treated with depot gonadotropin-releasing hormone analogs. J Clin Endocrinol Metab 2008, 93(7):2662-2669.
65. Bar A., Linder B., Sobel E.H., et al. Bayley-Pinneau method of height prediction in girls with central precocious puberty: correlation with adult height. J Pediatr 1995, 126(6):955-958.
66. Leger J., Reynaud R., Czernichow P. Do all girls with apparent idiopathic precocious puberty require gonadotropin-releasing hormone agonist treatment?. J Pediatr 2000, 137(6):819-825.
67. Paul D.L., Conte F.A., Grumbach M.M., et al. Long term effect of gonadotropin-releasing hormone agonist therapy in children with true precocious puberty treated at a median age of less than 5 years. J Clin Endocrinol Metab 1995, 80(2):546-551.
68. Kletter G.B., Kelch R.P. Clinical review 60. Effects of gonadotropin-releasing hormone analog therapy on adult stature in precocious puberty. J Clin Endocrinol Metab 1994, 79(2):331-334.
69. Arrigo T., Cisternino M., Galluzzi F., et al. Analysis of the factors affecting auxological response to GnRH agonist treatment and final height outcome in girls with idiopathic central precocious puberty. Eur J Endocrinol 1999, 141(2):140-144.
70. Oostdijk W., Rikken B., Schreuder S., et al. Final height in central precocious puberty after long term treatment with a slow release GnRH agonist. Arch Dis Child 1996, 75(4):292-297.
71. Galluzzi F., Salti R., Bindi G., et al. Adult height comparison between boys and girls with precocious puberty after long-term gonadotrophin-releasing hormone analogue therapy. Acta Paediatr 1998, 87(5):521-527.
72. Carel J.C., Roger M., Ispas S., et al. French study group of Decapeptyl in precocious puberty Final height after long-term treatment with triptorelin slow release for central precocious puberty: importance of statural growth after interruption of treatment. J Clin Endocrinol Metab 1999, 84(6):1973-1978.
73. Klein K.O., Barnes K.M., Jones J.V., et al. Increased final height in precocious puberty after long-term treatment with LHRH agonists: the National Institutes of Health experience. J Clin Endocrinol Metab 2001, 86(10):4711-4716.
74. Lazar L., Padoa A., Phillip M. Growth pattern and final height after cessation of gonadotropin-suppressive therapy in girls with central sexual precocity. J Clin Endocrinol Metab 2007, 92(9):3483-3489.
75. Cassio A., Cacciari E., Balsamo A., et al. Randomized trial of LHRH analogue treatment on final height in girls with onset of puberty aged 7.5-8.5 years. Arch Dis Child 1999, 81(4):329-332.
76. Bouvattier C., Coste J., Rodrigue D., et al. Lack of effect of GnRH agonists on final height in girls with advanced puberty: a randomized long-term pilot study. J Clin Endocrinol Metab 1999, 84(1):3575-3578.
77. Lazar L., Kauli R., Pertzelan A., et al. Gonadotropin-suppressive therapy in girls with early and fast puberty affects the pace of puberty but not total pubertal growth or final height. J Clin Endocrinol Metab 2002, 87(5):2090-2094.
78. Mul D., Bertelloni S., Carel J.C., et al. Effect of gonadotropin-releasing hormone agonist treatment in boys with central precocious puberty: final height results. Horm Res 2002, 58(1):1-7.
79. de Vries L., Guz-Mark A., Lazar L., et al. Premature thelarche: age at presentation affects clinical course but not clinical characteristics or risk to progress to precocious puberty. J Pediatr 2010, 156(3):466-471.
80. Oron T., Lebenthal Y., de Vries L., et al. Interrelationship of extent of precocious adrenarche in appropriate for gestational age girls with clinical outcome. J Pediatr 2012, 160(2):308-313.
81. Rosenfield R.L. Clinical review 6: diagnosis and management of delayed puberty. J Clin Endocrinol Metab 1990, 70(3):559-562.
82. Davenport M.L. Approach to the patient with Turner syndrome. J clin Endocrinol Metab 2010, 95(4):1487-1495.
83. Crowne E.C., Shalet S.M., Wallace W.H., et al. Final height in boys with untreated constitutional delay in growth and puberty. Arch Dis Child 1990, 65(10):1109-1112.
84. Albanese A., Stanhope R. Predictive factors in the determination of final height in boys with constitutional delay of growth and puberty. J Pediatr 1995, 126(4):545-550.
85. Strickland A.L., Underwood L.E., Voina S.J., et al. Growth retardation in Cushing's syndrome. Am J Dis Child 1972, 123(3):207-213.
86. Lee J.M., Kaciroti N., Appugliese D., et al. Body mass index and timing of pubertal initiation in boys. Arch Pediatr Adolesc Med 2010, 164(2):139-144.
87. Savage M.O., Preece M.A., Cameron N., et al. Gonadotrophin response to LH-RH in boys with delayed growth and adolescence. Arch Dis Child 1981, 56(7):552-556.
88. Zachmann M., Studer S., Prader A. Short-term testosterone treatment at bone age of 12 to 13 years does not reduce adult height in boys with constitutional delay of growth and adolescence. Helv Paediatr Acta 1987, 42(1):21-28.
89. Wilson D.M., Kei J., Hintz R.L., et al. Effects of testosterone therapy for pubertal delay. Am J Dis Child 1988, 142(1):96-99.
90. Kelly B.P., Paterson W.F., Donaldson M.D. Final height outcome and value of height prediction in boys with constitutional delay in growth and adolescence treated with intramuscular testosterone 125 mg per month for 3 months. Clin Endocrinol (Oxf) 2003, 58(3):267-272.
91. Wehkalampi K., Päkkilä K., Laine T., et al. Adult height in girls with delayed pubertal growth. Horm Res Paediatr 2011, 76(2):130-135.
92. Krajewska-Siuda E., Malecka-Tendera E., Krajewski-Siuda K. Are short boys with constitutional delay of growth and puberty candidates for rGH therapy according to FDA recommendations?. Horm Res 2006, 65(4):192-196.
93. Hero M., Wickman S., Dunkel L. Treatment with the aromatase inhibitor letrozole during adolescence increases near-final height in boys with constitutional delay of puberty. Clin Endocrinol (Oxf) 2006, 64(5):510-513.
94. Shulman D.I., Francis G.L., Palmert M.R., et al. Use of aromatase inhibitors in children and adolescents with disorders of growth and adolescent development. Pediatr 2008, 121(4):e975-e983.
95. Quigley C.A., Crowe B.J., Anglin D.G., et al. Growth hormone and low dose estrogen in Turner syndrome: results of a United States multi-center trial to near-final height. J Clin Endocrinol Metab 2002, 87(5):2033-2041.
96. Sperlich M., Butenandt O., Schwarz H.P. Final height and predicted height in boys with untreated constitutional growth delay. Eur J Pediatr 1995, 154(8):627-632.