Clinical Assessment of Sexual Maturation in Adolescents

REVIEW ARTICLE

Clinical assessment of sexual maturation in adolescents

Eugenio Chipkevitch*

Abstract Objective: to present the methods for clinical evaluation of sexual maturation in adolescents. Methods: bibliographic review concerning the practice of pubertal staging. Results: the assessment of sexual maturation is an essential step in the comprehensive health care of adolescents, allowing for the evaluation of their developmental stage. In addition, this assessment allows establishing a correlation between different pubertal events, following up diseases, and interpreting laboratory tests appropriately. Pubertal stage is assessed by the examination of breasts and pubic hair in females, and genitals and pubic hair in males. A new photographic standard for pubertal staging and a new method for clinical measurement of testicular volume are presented. Conclusions: the assessment of sexual maturation is an important feature in the health care of adolescent patients and must be included in the clinical practice of pediatricians involved in adolescent medicine.

J Pediatr (Rio J) 2001; 77 (Supl. 2): S135-S142: adolescence, puberty, sex maturation.

Introduction Puberty is a period of biological maturation marked by In adolescence, chronological age is not a reliable the appearance of secondary sexual characteristics, growth parameter for biological, psychological, and social spurt, and changes in body composition. With the exception characterization of individuals. Adolescents with the same of the fetal period, there is no other stage in human age are frequently in different stages of puberty considering development in which height growth and changes in body that its onset and progression are highly variable. Most composition are as intense and rapid as during puberty. The pubertal events (maximum growth velocity, menarche, final growth spurt, for example, lasts three to four years and height, and so on) and most pathologies associated to represents approximately a 20% and 50% gain in relation to puberty (acne, scoliosis, gynecomasty, and so on) are more adult height and weight, respectively.1 often correlated to specific stages of puberty than to chronological age.1 Pubertal staging allows doctors to assess the maturation of adolescent patients; to correlate several pubertal phenomena; to estimate age at menarche, growth spurt, and final height; to offer early orientation to * Director of the Paulista Institute for Adolescence, former director of the Adolescent services of the Children’s Hospital Darcy Vargas, São Paulo. youngsters in relation to upcoming pubertal events; to offer

S135 S136 Jornal de Pediatria - Vol. 77, Supl.2, 2001 Clinical assessment of sexual maturation... - Chipkevitch E advice on choice of proper sports modalities; to assess exams properly; and to treat pathologies associated to Table 1 - Sexual maturity rating puberty.1 Male genitals In this sense, pubertal staging is an important measure for characterizing the maturation of adolescents and for G1 Childlike penis, testicles, and scrotum. easier understanding and handling of the most common G2 Initial increase in testicular volume (>4ml). The clinical problems for this age group. Our objective is to texture of the scrotal skin becomes reddened offer a brief review on the practice of pubertal staging, and and thinner. The enlargement of the penis is to present a new photographic model on the stages of sexual minimal or absent. maturation and a new method for measurement of testicular G3 Increased length of the penis. Great enlargement volume. of testicles and scrotum. G4 Increased length and circumference of the penis with great enlargement of the glans. Enlarged Pubertal staging testicles and scrotum, and increased scrotal skin pigmentation. Though certain models of pubertal staging had already been proposed during the 1940s and 1950s,2-4 doctor J.M. G5 Full development of genital organs, with adult appearance. Tanner was the one who presented a standardized method 5 for staging of sexual maturation, which became widely Breasts (females) used during the 1960s and is still the most widely used method. M1 Childlike, with elevated papilla. Staging of sexual maturation is carried out with breast M2 Breast bud: initial increase of the mammary and pubic hair growth examination for girls, and with gland, with elevated areola and papilla, forming genital and pubic hair growth for boys. Breasts and genitals a small mound. Areolar diameter and texture change. are examined according to size, shape, and characteristics and pubic hair according to quantity and distribution (Table M3 Great enlargement of the breasts and areola, 1). Stage 1 (Tanner 1) corresponds to the prepubertal phase without contour separation. and stage 5 (Tanner 5) corresponds to late-pubertal (adult) M4 Greater enlargement of the breast and areola. A phase. In this sense, stages 2, 3, and 4, or the midpubertal second mound is formed above the breast stages, represent puberty. Stages 2 to 4 are conventionally contour. called sexual maturation stages, or Tanner stages. M5 Adult mature breasts. Recession of areola to the The classical work of Tanner included a set of black- mound of breast tissue. and-white photographs for illustration of each maturation stage for both sexes.5 A few years later, a Dutch group Pubic hair (both sexes) published a set of color photographs for these same stages.6 P1 No pubic hair. Vellus over the pubes in no In this article, we reproduce our black-and-white model for further developed than that over the abdominal sexual maturation (Figures 1, 2, 3, and 4) originally published wall. in 1995.1 This is the first published Brazilian model and the P2 There is sparse growth of long, slightly third in the international literature. pigmented, downy hair, straight or only slightly For each sex, staging is carried out according to two curled, appearing chiefly at base of penis or steps: breasts (B) and pubic hair (P) growth for girls, and along the labia majora). genitals (G) and pubic hair (P) for boys (Table 1). It is P3 Hair is considerably darker, coarser, and more recommended to always assess these two steps separately; curled, and spreads sparsely over junction of for example, B3P3 instead of stage 3. Adolescents may be pubes. in different maturation stages for each of the two P4 Hair is now adult in type but there is no spread characteristics, for example, B4P5 or G2P1 considering to the inner thighs. that maturation of the characteristics depends on different P5 Adult quantity and distribution with hair present hormonal and genetic mechanisms. Pubertal events correlate on inner thighs. differently to specific components of maturation staging; P6 Hair spreads above the pubes. for example, age at menarche is more correlated to breast development than to pubic hair growth. Most adolescents do not present differences of more than one stage between B and G in relation to P; however, situations of G1P3, G4P1, or M3P1, though rare, can be observed in normal During puberty, there is an increment in nipple (papilla) adolescents. Nevertheless, important differences as such and nipple areola in both girls and boys, but especially in the can also be an indication of a pathology (supra-renal, earlier. The increment in nipple diameter is greater during testicular, etc).7 stages B4 and B5, which helps to differentiate stages B3, Clinical assessment of sexual maturation... - Chipkevitch E Jornal de Pediatria - Vol. 77, Supl.2 , 2001 S137

Figure 1 - Stages of sexual maturation in males - genitals S138 Jornal de Pediatria - Vol. 77, Supl.2, 2001 Clinical assessment of sexual maturation... - Chipkevitch E

Figure 2 - Stages of sexual maturation in males - pubic hair Clinical assessment of sexual maturation... - Chipkevitch E Jornal de Pediatria - Vol. 77, Supl.2 , 2001 S139

Figure 3 - Stages of sexual maturation in females - breasts S140 Jornal de Pediatria - Vol. 77, Supl.2, 2001 Clinical assessment of sexual maturation... - Chipkevitch E

Figure 4 - Stages of sexual maturation in females - pubic hair Clinical assessment of sexual maturation... - Chipkevitch E Jornal de Pediatria - Vol. 77, Supl.2 , 2001 S141

B4, and B5. The nipple presents little increase between stages 1 and 3 and marked increase between stages B3 and B4 (diameter averages of 3 mm for B1; 3.4 mm for B2; 4.7 mm for B3; 7.3 mm for B4; and 9.4 mm for B5).7,8 Initially, the appearance of thelarche (B2) may occur in only one breast; the contralateral breast will usually start growing weeks or months later. Breast asymmetries, however, can persist for some time between B2 and B4 or, in some women, be permanent. The stage B4 is not observed in all girls; apparently, some female individuals go directly from B3 to B5 or stage B4 occurs so rapidly that it is not registered in successive medical appointments. Conversely, in other girls breast development may stop in stage B4. The stage 6 of pubic hair growth is observed in approximately 80% of men and 10% of women; in certain individuals, it will only be complete years after puberty is over.

Testicular volume The measurement of testicular volume represents an additional instrument for assessment of male sexual maturation. The most widely used method for measuring testicular volume uses the Prader orchidometer, which includes 12 ellipsoid testicular models made of wood or plastic and attached to a string. The models have volumes of one to 25 ml.9 To assess testicular volume, the doctor palpates the testis with one hand while holding the orchidometer in the other, examining the patient for the model that is more similar to the palpated testis. Takihara et al.10 proposed a new orchidometer that consists of a graded series of punched-out elliptical rings with the volume of the ellipsoids indicated on each ring for volumes of 1 to 30 ml. Considering that orchidometers are not easily available in our setting, other methods that offer similar precision can be applied. Thus, it is also possible to measure the two axes of the testis with a transparent ruler or, better yet, with a caliper (similar to that used for measurement of skinfold) and calculate the volume using the formula V = 0.523 x L Figure 5 - Scheme for graphic measurement of testicular x C2 (with V for volume, L for longitudinal diameter, and C volume. The testicle is palpated and visually for cross-sectional diameter). compared with the graphic models. Testicular volume is determined according to one of the six volumes or The measurement of testicular volume by one of the intermediate volumes between two ultrasonography employs the same principle, though it has consecutive volumes depicted . The entire been reported as the most precise method.11 We were able measurement scale includes 13 volumes: less than to show, in a different article, that all methods offer 2ml, 2ml, 3.5ml, 5ml, 7.5ml, 10ml, 12.5ml, 15ml, comparable reliability as long as the volumes obtained are 17.5ml, 20ml, 22.5ml, 25ml, and greater than 25ml corrected using the equations of the linear structural model.12 In this sense, it was possible to propose a method for visual comparison of the palpated testes with graphic models for estimation of testicular volume (Figure 5); this new proposed In general, the testes of children have one to two, and method is, thus, simple and its reliability comparable to that sometimes three, ml in volume. Testes with four ml or more of orchidometer and ultrasonography.12 are, almost as a rule, characteristic of puberty. Consequently, S142 Jornal de Pediatria - Vol. 77, Supl.2, 2001 Clinical assessment of sexual maturation... - Chipkevitch E attaining a volume of four ml or more is an indication of G2; 2. Schonfeld WA. Primary and secondary sexual characteristics: this is an example of how measurement of testicular volume Study of their development in males from birth to maturity, with can help to carry out pubertal staging. A testicular volume biometric study of penis and testes. Am J Dis Child 1943; 65: 535-49. of three ml is generally prognostic of puberty, for an 3. Reynolds EL, Wines JV. Individual differences in physical estimated 80% chance of starting within the following six changes associated with adolescence in girls. Am J Dis Child 7 months. Eleven to 12-year old boys with small testes (one 1948; 75:329-50. to two ml) are probably affected by delay of pubertal 4. Reynolds EL, Wines JV. Individual differences in physical development (usually constitutional). changes associated with adolescence in boys. Am J Dis Child Measuring testicular volume is also important for the 1951; 82:529-47. assessment of diagnosis of certain pathologies; for example, 5. Tanner JM. Growth at adolescence. Oxford: Blackwell; 1962. cases of Klinefelter syndrome (small testes) or of Fragile- 6. van Weringen JC, Waffelbakker F, Verbrugge HP. Growth X syndrome (possible macro-orchidism). The follow-up Diagrams, 1965, Netherlands. Leiden: Netherland Institute for Preventive Medicine; 1971. measurement of testicular volume is important in postsurgical 7. Wilson JD, Foster DW, Kronenberg HM, Williams RH, ed. follow-up of orchipexy (to check whether ectopy, twisting Williams Textbook of Endocrinology. 9th ed. Philadelphia: Saun- and/or surgical handling has affected testicular development) ders; 1998; p.1509-625. or of varicocele (that presents risk for testicular hypertrophy 8. Kreipe RE. Normal somatic adolescent growth and development. and subfertility). In: McAnarney ER, Kreipe RE, Orr DP, Comerci GD, eds. Most adolescents have similar left- and right-hand side Textbook of Adolescent Medicine. Philadelphia: Saunders; 1992; testicular volumes; however, it is common for the left-hand p.44-67. side testicle to have a slightly lower volume than the right- 9. Prader A. Testicular size: Assessment and clinical importance. Triangle 1966; 7:240-3. hand side one. In cases of significant differences (20%), it 10. Takihara H, Cosentino MJ, Sakatoku J, Cockett ATK. Signifi- is important to examine the patient for factors that may be cance of testicular size measurement in andrology: I. A new interfering in growth of the smaller testis (varicocele, orchidometer and its clinical application. Fertil Steril 1983; 39: previous surgery, orchitis, twisting, etc). 836-40. Testicular volume is significantly correlated with the 11. Behre HM, Nashan D, Nieschlag E. Objective measurement of testicular function. Some authors consider a testicular volume testicular volume by ultrasonography: evaluation of the tech- nique and comparison with orchidometer estimates. Int J Androl of 12 ml, attained, in average, around 13 to 14 years of age 1989; 12:395. and during maximum growth velocity, the minimum volume 12. Chipkevitch E, Nishimura RT, Tu DGS, Galea-Rojas M. Clinical compatible with fertility; in this sense, attainment of this measurement of testicular volume in adolescents: Comparison of volume is comparable to menarche as a reference for male the reliability of 5 methods. J Urol 1996; 156:2050-3. sexual maturity.1 The average testicular volume of Brazilian adolescents is four ml for G2, nine ml for G3, 16 ml for G4, and 20 ml for G5. However, there can be significant variations in these values. Consequently, a specific testicular volume cannot be used to define stage of sexual maturation. Adult testes, Correspondence: for example, can vary from 12 to 30 ml in volume.7 Dr. Eugenio Chipkevitch Instituto Paulista de Adolescência Rua Alcides Ricardini Neves, 12 - cjs. 906-909 References CEP 04575-050 – São Paulo, SP, Brazil 1. Chipkevitch E. Puberdade e adolescência: aspectos biológicos, Phone/fax: + 55 11 5506.9005 clínicos e psicossociais. São Paulo: Roca; 1995. E-mail: [email protected]