UpToDate
Official reprint from UpToDate®
www.uptodate.com ©2016 UpToDate®

Normal puberty

Authors
Frank M Biro, MD
Yee-Ming Chan, MD, PhD
Section Editors
Teresa K Duryea, MD
Peter J Snyder, MD
Mitchell E Geffner, MD
Diane Blake, MD
Deputy Editor
Alison G Hoppin, MD

INTRODUCTION

Adolescents experience several types of maturation, including cognitive (the development of formal operational thought), psychosocial (the stages of adolescence), and physical. This complex series of physical transitions is known as puberty, and these changes may impact psychosocial factors.

The most visible changes during puberty are growth in stature and development of secondary sexual characteristics. Equally profound are changes in body composition; the achievement of fertility; and changes in most body systems, such as the neuroendocrine axis, and bone size and mineralization; and the cardiovascular system. As an example, puberty is associated with cardiovascular changes, including greater aerobic power reserve, electrocardiographic changes, and blood pressure changes.

The normal sequence of pubertal events and perils of puberty are reviewed here. Precocious and delayed puberty are discussed separately. (See "Definition, etiology, and evaluation of precocious puberty" and "Diagnosis and treatment of delayed puberty".)

DEFINITIONS

Puberty is the general term for the transition from sexual immaturity to sexual maturity. There are two main physiological events in puberty:

Gonadarche is the activation of the gonads by the pituitary hormones follicle-stimulating hormone (FSH) and luteinizing hormone (LH).

                          

Subscribers log in here

To continue reading this article, you must log in with your personal, hospital, or group practice subscription. For more information or to purchase a personal subscription, click below on the option that best describes you:
Literature review current through: Nov 2016. | This topic last updated: Tue Apr 19 00:00:00 GMT+00:00 2016.
The content on the UpToDate website is not intended nor recommended as a substitute for medical advice, diagnosis, or treatment. Always seek the advice of your own physician or other qualified health care professional regarding any medical questions or conditions. The use of this website is governed by the UpToDate Terms of Use ©2016 UpToDate, Inc.
References
Top
  1. Laron Z. Age at first ejaculation (spermarche)--the overlooked milestone in male development. Pediatr Endocrinol Rev 2010; 7:256.
  2. Tanner JM, Davies PS. Clinical longitudinal standards for height and height velocity for North American children. J Pediatr 1985; 107:317.
  3. Herman-Giddens ME, Slora EJ, Wasserman RC, et al. Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in Office Settings network. Pediatrics 1997; 99:505.
  4. Biro FM, Greenspan LC, Galvez MP, et al. Onset of breast development in a longitudinal cohort. Pediatrics 2013; 132:1019.
  5. Sun SS, Schubert CM, Chumlea WC, et al. National estimates of the timing of sexual maturation and racial differences among US children. Pediatrics 2002; 110:911.
  6. Herman-Giddens ME, Steffes J, Harris D, et al. Secondary sexual characteristics in boys: data from the Pediatric Research in Office Settings Network. Pediatrics 2012; 130:e1058.
  7. Karpati AM, Rubin CH, Kieszak SM, et al. Stature and pubertal stage assessment in American boys: the 1988-1994 Third National Health and Nutrition Examination Survey. J Adolesc Health 2002; 30:205.
  8. Sun SS, Schubert CM, Liang R, et al. Is sexual maturity occurring earlier among U.S. children? J Adolesc Health 2005; 37:345.
  9. Wu FC, Butler GE, Kelnar CJ, Sellar RE. Patterns of pulsatile luteinizing hormone secretion before and during the onset of puberty in boys: a study using an immunoradiometric assay. J Clin Endocrinol Metab 1990; 70:629.
  10. Cutler GB Jr, Loriaux DL. Andrenarche and its relationship to the onset of puberty. Fed Proc 1980; 39:2384.
  11. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child 1969; 44:291.
  12. Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child 1970; 45:13.
  13. Kaplowitz PB, Oberfield SE. Reexamination of the age limit for defining when puberty is precocious in girls in the United States: implications for evaluation and treatment. Drug and Therapeutics and Executive Committees of the Lawson Wilkins Pediatric Endocrine Society. Pediatrics 1999; 104:936.
  14. Biro FM, McMahon RP, Striegel-Moore R, et al. Impact of timing of pubertal maturation on growth in black and white female adolescents: The National Heart, Lung, and Blood Institute Growth and Health Study. J Pediatr 2001; 138:636.
  15. Garn SM, LaVelle M, Rosenberg KR, Hawthorne VM. Maturational timing as a factor in female fatness and obesity. Am J Clin Nutr 1986; 43:879.
  16. Abbassi V. Growth and normal puberty. Pediatrics 1998; 102:507.
  17. Bass S, Delmas PD, Pearce G, et al. The differing tempo of growth in bone size, mass, and density in girls is region-specific. J Clin Invest 1999; 104:795.
  18. Berkey CS, Dockery DW, Wang X, et al. Longitudinal height velocity standards for U.S. adolescents. Stat Med 1993; 12:403.
  19. Biro FM, Huang B, Crawford PB, et al. Pubertal correlates in black and white girls. J Pediatr 2006; 148:234.
  20. Huang B, Biro FM, Dorn LD. Determination of relative timing of pubertal maturation through ordinal logistic modeling: evaluation of growth and timing parameters. J Adolesc Health 2009; 45:383.
  21. Lorentzon M, Norjavaara E, Kindblom JM. Pubertal timing predicts leg length and childhood body mass index predicts sitting height in young adult men. J Pediatr 2011; 158:452.
  22. Magarey AM, Boulton TJ, Chatterton BE, et al. Bone growth from 11 to 17 years: relationship to growth, gender and changes with pubertal status including timing of menarche. Acta Paediatr 1999; 88:139.
  23. McKay HA, Bailey DA, Mirwald RL, et al. Peak bone mineral accrual and age at menarche in adolescent girls: a 6-year longitudinal study. J Pediatr 1998; 133:682.
  24. Taranger J, Engström I, Lichtenstein H, Svennberg- Redegren I. VI. Somatic pubertal development. Acta Paediatr Scand Suppl 1976; :121.
  25. Lloyd T, Rollings N, Andon MB, et al. Determinants of bone density in young women. I. Relationships among pubertal development, total body bone mass, and total body bone density in premenarchal females. J Clin Endocrinol Metab 1992; 75:383.
  26. Gilsanz V, Roe TF, Mora S, et al. Changes in vertebral bone density in black girls and white girls during childhood and puberty. N Engl J Med 1991; 325:1597.
  27. Maynard LM, Wisemandle W, Roche AF, et al. Childhood body composition in relation to body mass index. Pediatrics 2001; 107:344.
  28. Gasser T, Ziegler P, Kneip A, et al. The dynamics of growth of weight, circumferences and skinfolds in distance, velocity and acceleration. Ann Hum Biol 1993; 20:239.
  29. Tirosh A, Shai I, Afek A, et al. Adolescent BMI trajectory and risk of diabetes versus coronary disease. N Engl J Med 2011; 364:1315.
  30. Whitaker RC, Wright JA, Pepe MS, et al. Predicting obesity in young adulthood from childhood and parental obesity. N Engl J Med 1997; 337:869.
  31. Baker JL, Olsen LW, Sørensen TI. [Childhood body mass index and the risk of coronary heart disease in adulthood]. Ugeskr Laeger 2008; 170:2434.
  32. Susman EJ, Houts RM, Steinberg L, et al. Longitudinal development of secondary sexual characteristics in girls and boys between ages 91/2 and 151/2 years. Arch Pediatr Adolesc Med 2010; 164:166.
  33. Ogland B, Nilsen ST, Forman MR, Vatten LJ. Pubertal development in daughters of women with pre-eclampsia. Arch Dis Child 2011; 96:740.
  34. Ibáñez L, de Zegher F. Puberty after prenatal growth restraint. Horm Res 2006; 65 Suppl 3:112.
  35. Biro FM, Lucky AW, Simbartl LA, et al. Pubertal maturation in girls and the relationship to anthropometric changes: pathways through puberty. J Pediatr 2003; 142:643.
  36. Rosenfield RL, Lipton RB, Drum ML. Thelarche, pubarche, and menarche attainment in children with normal and elevated body mass index. Pediatrics 2009; 123:84.
  37. Wellens R, Malina R, Roche A , et al. Body size and fatness in young adults in relation to age at menarche. Am J Hum Biol 1992; 4:783.
  38. Kaplowitz PB, Slora EJ, Wasserman RC, et al. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics 2001; 108:347.
  39. Freedman DS, Khan LK, Serdula MK, et al. The relation of menarcheal age to obesity in childhood and adulthood: the Bogalusa heart study. BMC Pediatr 2003; 3:3.
  40. Biro FM, Lucky AW, Huster GA, Morrison JA. Pubertal staging in boys. J Pediatr 1995; 127:100.
  41. Tomova A, Deepinder F, Robeva R, et al. Growth and development of male external genitalia: a cross-sectional study of 6200 males aged 0 to 19 years. Arch Pediatr Adolesc Med 2010; 164:1152.
  42. Sørensen K, Aksglaede L, Petersen JH, Juul A. Recent changes in pubertal timing in healthy Danish boys: associations with body mass index. J Clin Endocrinol Metab 2010; 95:263.
  43. Liu YX, Wikland KA, Karlberg J. New reference for the age at childhood onset of growth and secular trend in the timing of puberty in Swedish. Acta Paediatr 2000; 89:637.
  44. Ma HM, Chen SK, Chen RM, et al. Pubertal development timing in urban Chinese boys. Int J Androl 2011; 34:e435.
  45. Goldstein JR. A secular trend toward earlier male sexual maturity: evidence from shifting ages of male young adult mortality. PLoS One 2011; 6:e14826.
  46. Monteilh C, Kieszak S, Flanders WD, et al. Timing of maturation and predictors of Tanner stage transitions in boys enrolled in a contemporary British cohort. Paediatr Perinat Epidemiol 2011; 25:75.
  47. Sandhu J, Ben-Shlomo Y, Cole TJ, et al. The impact of childhood body mass index on timing of puberty, adult stature and obesity: a follow-up study based on adolescent anthropometry recorded at Christ's Hospital (1936-1964). Int J Obes (Lond) 2006; 30:14.
  48. Boyne MS, Thame M, Osmond C, et al. Growth, body composition, and the onset of puberty: longitudinal observations in Afro-Caribbean children. J Clin Endocrinol Metab 2010; 95:3194.
  49. Lee JM, Kaciroti N, Appugliese D, et al. Body mass index and timing of pubertal initiation in boys. Arch Pediatr Adolesc Med 2010; 164:139.
  50. Wang Y. Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls. Pediatrics 2002; 110:903.
  51. Kleber M, Schwarz A, Reinehr T. Obesity in children and adolescents: relationship to growth, pubarche, menarche, and voice break. J Pediatr Endocrinol Metab 2011; 24:125.
  52. Lee JM, Wasserman R, Kaciroti N, et al. Timing of Puberty in Overweight Versus Obese Boys. Pediatrics 2016; 137:e20150164.
  53. Biro FM, Pinney SM, Huang B, et al. Hormone changes in peripubertal girls. J Clin Endocrinol Metab 2014; 99:3829.
  54. Midyett LK, Moore WV, Jacobson JD. Are pubertal changes in girls before age 8 benign? Pediatrics 2003; 111:47.
  55. Ellis BJ, Garber J. Psychosocial antecedents of variation in girls' pubertal timing: maternal depression, stepfather presence, and marital and family stress. Child Dev 2000; 71:485.
  56. Boynton-Jarrett R, Harville EW. A prospective study of childhood social hardships and age at menarche. Ann Epidemiol 2012; 22:731.
  57. Vandenbergh JG. Social determinants of the onset of puberty in rodents. J Sex Res 1974; 10:181.
  58. Freedman DS, Khan LK, Serdula MK, et al. Relation of age at menarche to race, time period, and anthropometric dimensions: the Bogalusa Heart Study. Pediatrics 2002; 110:e43.
  59. Buck Louis GM, Gray LE Jr, Marcus M, et al. Environmental factors and puberty timing: expert panel research needs. Pediatrics 2008; 121 Suppl 3:S192.
  60. Adair LS, Gordon-Larsen P. Maturational timing and overweight prevalence in US adolescent girls. Am J Public Health 2001; 91:642.
  61. Frisch R, Revelle R. Variation in body weights and the age of the adolescent growth spurt among Latin American and Asian populations, in relation to calorie supplies. Hum Biol 1969; 41:185.
  62. Frisch RE, Revelle R, Cook S. Components of weight at menarche and the initiation of the adolescent growth spurt in girls: estimated total water, llean body weight and fat. Hum Biol 1973; 45:469.
  63. Grumbach MM, Sizonenko PC, Aubert ML. Control of the onset of puberty, Williams & Wilkins, Baltimore 1990.
  64. Ahima RS, Prabakaran D, Mantzoros C, et al. Role of leptin in the neuroendocrine response to fasting. Nature 1996; 382:250.
  65. Farooqi IS, Matarese G, Lord GM, et al. Beneficial effects of leptin on obesity, T cell hyporesponsiveness, and neuroendocrine/metabolic dysfunction of human congenital leptin deficiency. J Clin Invest 2002; 110:1093.
  66. 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.
  67. Roemmich JN, Rogol AD. Role of leptin during childhood growth and development. Endocrinol Metab Clin North Am 1999; 28:749.
  68. Mantzoros CS, Flier JS, Rogol AD. A longitudinal assessment of hormonal and physical alterations during normal puberty in boys. V. Rising leptin levels may signal the onset of puberty. J Clin Endocrinol Metab 1997; 82:1066.
  69. Ahmed ML, Ong KK, Morrell DJ, et al. Longitudinal study of leptin concentrations during puberty: sex differences and relationship to changes in body composition. J Clin Endocrinol Metab 1999; 84:899.
  70. Horlick MB, Rosenbaum M, Nicolson M, et al. Effect of puberty on the relationship between circulating leptin and body composition. J Clin Endocrinol Metab 2000; 85:2509.
  71. Kratzsch J, Lammert A, Bottner A, et al. Circulating soluble leptin receptor and free leptin index during childhood, puberty, and adolescence. J Clin Endocrinol Metab 2002; 87:4587.
  72. Kasuya E, Nyberg CL, Mogi K, Terasawa E. A role of gamma-amino butyric acid (GABA) and glutamate in control of puberty in female rhesus monkeys: effect of an antisense oligodeoxynucleotide for GAD67 messenger ribonucleic acid and MK801 on luteinizing hormone-releasing hormone release. Endocrinology 1999; 140:705.
  73. Seminara SB, Crowley WF Jr. Kisspeptin and GPR54: discovery of a novel pathway in reproduction. J Neuroendocrinol 2008; 20:727.
  74. Lippincott MF, True C, Seminara SB. Use of genetic models of idiopathic hypogonadotrophic hypogonadism in mice and men to understand the mechanisms of disease. Exp Physiol 2013; 98:1522.
  75. de Roux N, Genin E, Carel JC, et al. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A 2003; 100:10972.
  76. Topaloglu AK, Tello JA, Kotan LD, et al. Inactivating KISS1 mutation and hypogonadotropic hypogonadism. N Engl J Med 2012; 366:629.
  77. Shahab M, Mastronardi C, Seminara SB, et al. Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci U S A 2005; 102:2129.
  78. Gianetti E, Tusset C, Noel SD, et al. TAC3/TACR3 mutations reveal preferential activation of gonadotropin-releasing hormone release by neurokinin B in neonatal life followed by reversal in adulthood. J Clin Endocrinol Metab 2010; 95:2857.
  79. Mitsushima D, Hei DL, Terasawa E. gamma-Aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty. Proc Natl Acad Sci U S A 1994; 91:395.
  80. Keen KL, Burich AJ, Mitsushima D, et al. Effects of pulsatile infusion of the GABA(A) receptor blocker bicuculline on the onset of puberty in female rhesus monkeys. Endocrinology 1999; 140:5257.
  81. Abreu AP, Dauber A, Macedo DB, et al. Central precocious puberty caused by mutations in the imprinted gene MKRN3. N Engl J Med 2013; 368:2467.
  82. Elks CE, Perry JR, Sulem P, et al. Thirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies. Nat Genet 2010; 42:1077.
  83. Sulem P, Gudbjartsson DF, Rafnar T, et al. Genome-wide association study identifies sequence variants on 6q21 associated with age at menarche. Nat Genet 2009; 41:734.
  84. Perry JR, Stolk L, Franceschini N, et al. Meta-analysis of genome-wide association data identifies two loci influencing age at menarche. Nat Genet 2009; 41:648.
  85. Ong KK, Elks CE, Li S, et al. Genetic variation in LIN28B is associated with the timing of puberty. Nat Genet 2009; 41:729.
  86. Perry JR, Day F, Elks CE, et al. Parent-of-origin-specific allelic associations among 106 genomic loci for age at menarche. Nature 2014; 514:92.
  87. Looker AC, Dallman PR, Carroll MD, et al. Prevalence of iron deficiency in the United States. JAMA 1997; 277:973.
  88. Daniel WA Jr. Hematocrit: maturity relationship in adolescence. Pediatrics 1973; 52:388.
  89. Bergström E, Hernell O, Lönnerdal B, Persson LA. Sex differences in iron stores of adolescents: what is normal? J Pediatr Gastroenterol Nutr 1995; 20:215.
  90. Biro F, Lucky A, Huster G, et al. Difficulties in differentiating transient from persistent gynecomastia in adolescents. Pediatr Res 1990; 27:3A.
  91. Biro F. Gynecomastia. In: Ambulatory Pediatric Care, Dershewitz R (Ed), Lippincott-Raven, Philadelphia 1999. p.516.
  92. Lucky AW, Biro FM, Huster GA, et al. Acne vulgaris in early adolescent boys. Correlations with pubertal maturation and age. Arch Dermatol 1991; 127:210.
  93. Lucky AW, Biro FM, Simbartl LA, et al. Predictors of severity of acne vulgaris in young adolescent girls: results of a five-year longitudinal study. J Pediatr 1997; 130:30.
  94. Joinson C, Heron J, Lewis G, et al. Timing of menarche and depressive symptoms in adolescent girls from a UK cohort. Br J Psychiatry 2011; 198:17.
  95. Orr DP, Brack CJ, Ingersoll G. Pubertal maturation and cognitive maturity in adolescents. J Adolesc Health Care 1988; 9:273.
  96. Angold A, Worthman CW. Puberty onset of gender differences in rates of depression: a developmental, epidemiologic and neuroendocrine perspective. J Affect Disord 1993; 29:145.
  97. Brown KM, McMahon RP, Biro FM, et al. Changes in self-esteem in black and white girls between the ages of 9 and 14 years. The NHLBI Growth and Health Study. J Adolesc Health 1998; 23:7.
  98. Striegel-Moore RH, McMahon RP, Biro FM, et al. Exploring the relationship between timing of menarche and eating disorder symptoms in Black and White adolescent girls. Int J Eat Disord 2001; 30:421.
  99. Graber JA, Lewinsohn PM, Seeley JR, Brooks-Gunn J. Is psychopathology associated with the timing of pubertal development? J Am Acad Child Adolesc Psychiatry 1997; 36:1768.
  100. Magnusson D, Stattin H, Allen V. Differential maturation among girls and its relation to social adjustment: A longitudinal perspective. In: Life-Span Development and Behavior, Featerman D, Lerner R (Eds), Academic Press, New York 1986. p.135.
  101. Ge X, Conger RD, Elder GH Jr. Coming of age too early: pubertal influences on girls' vulnerability to psychological distress. Child Dev 1996; 67:3386.
  102. Dahl RE. Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann N Y Acad Sci 2004; 1021:1.
  103. Giedd JN. Structural magnetic resonance imaging of the adolescent brain. Ann N Y Acad Sci 2004; 1021:77.
  104. Backous DD, Farrow JA, Friedl KE. Assessment of pubertal maturity in boys, using height and grip strength. J Adolesc Health Care 1990; 11:497.
  105. Bailey DA, Wedge JH, McCulloch RG, et al. Epidemiology of fractures of the distal end of the radius in children as associated with growth. J Bone Joint Surg Am 1989; 71:1225.
  106. Legro RS, Lin HM, Demers LM, Lloyd T. Rapid maturation of the reproductive axis during perimenarche independent of body composition. J Clin Endocrinol Metab 2000; 85:1021.
  107. Apter D, Vihko R. Early menarche, a risk factor for breast cancer, indicates early onset of ovulatory cycles. J Clin Endocrinol Metab 1983; 57:82.
  108. Tanner J. Growth at Adolescence, Blackwell Scientific Publications, Oxford 1962.
  109. Gevelber MA, Biro FM. Adolescents and sexually transmitted diseases. Pediatr Clin North Am 1999; 46:747.
  110. Rosenthal SL, Biro FM, Succop PA, et al. Impact of demographics, sexual history, and psychological functioning on the acquisition of STDS in adolescents. Adolescence 1997; 32:757.
  111. Harrison HR, Costin M, Meder JB, et al. Cervical Chlamydia trachomatis infection in university women: relationship to history, contraception, ectopy, and cervicitis. Am J Obstet Gynecol 1985; 153:244.
  112. Moscicki AB, Winkler B, Irwin CE Jr, Schachter J. Differences in biologic maturation, sexual behavior, and sexually transmitted disease between adolescents with and without cervical intraepithelial neoplasia. J Pediatr 1989; 115:487.
  113. Shew ML, Fortenberry JD, Miles P, Amortegui AJ. Interval between menarche and first sexual intercourse, related to risk of human papillomavirus infection. J Pediatr 1994; 125:661.