Introduction

Puberty is a period of biological maturation marked by the appearance of secondary sexual characteristics, growth spurt, and changes in body composition. With the exception of the fetal period, there is no other stage in human development in which height growth and changes in body composition are as intense and rapid as during puberty. The growth spurt, for example, lasts three to four years and represents approximately a 20% and 50% gain in relation to adult height and weight, respectively(1).

In adolescence, chronological age is not a reliable parameter for biological, psychological, and social characterization of individuals. Adolescents with the same age are frequently in different stages of puberty considering that its onset and progression are highly variable. Most pubertal events (maximum growth velocity, menarche, final height, and so on) and most pathologies associated to puberty (acne, scoliosis, gynecomasty, and so on) are more 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 youngsters in relation to upcoming pubertal events; to offer advice on choice of proper sports modalities; to assess exams properly; and to treat pathologies associated to puberty(1).

In this sense, pubertal staging is an important measure for characterizing the maturation of adolescents and for easier understanding and handling of the most common clinical problems for this age group. Our objective is to offer a brief review on the practice of pubertal staging, and to present a new photographic model on the stages of sexual maturation and a new method for measurement of testicular volume.

Pubertal staging

Though certain models of pubertal staging had already been proposed during the 1940s and 1950s(2-4), doctor J.M. Tanner was the one who presented a standardized method for staging of sexual maturation(5), which became widely used during the 1960s and is still the most widely used method.

Staging of sexual maturation is carried out with breast and pubic hair growth examination for girls, and with genital and pubic hair growth for boys. Breasts and genitals are examined according to size, shape, and characteristics and pubic hair according to quantity and distribution (Table 1). Stage 1 (Tanner 1) corresponds to the prepubertal phase and stage 5 (Tanner 5) corresponds to late-pubertal (adult) phase. In this sense, stages 2, 3, and 4, or the midpubertal stages, represent puberty. Stages 2 to 4 are conventionally called sexual maturation stages, or Tanner stages.

Table 1 -
Sexual maturity rating

The classical work of Tanner included a set of black-and-white photographs for illustration of each maturation stage for both sexes(5). A few years later, a Dutch group published a set of color photographs for these same stages(6). In this article, we reproduce our black-and-white model for sexual maturation (Figures 1, 2, 3, and 4) originally published in 1995(1). This is the first published Brazilian model and the third in the international literature.

Figure 1 -
Stages of sexual maturation in males - genitals

Figure 2 -
Stages of sexual maturation in males - pubic hair

Figure 3 -
Stages of sexual maturation in females - breasts

Figure 4 -
Stages of sexual maturation in females - pubic hair

For each sex, staging is carried out according to two steps: breasts (B) and pubic hair (P) growth for girls, and genitals (G) and pubic hair (P) for boys (Table 1). It is recommended to always assess these two steps separately; for example, B3P3 instead of stage 3. Adolescents may be in different maturation stages for each of the two characteristics, for example, B4P5 or G2P1 considering that maturation of the characteristics depends on different hormonal and genetic mechanisms. Pubertal events correlate differently to specific components of maturation staging; 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 adolescents. Nevertheless, important differences as such can also be an indication of a pathology (supra-renal, testicular, etc)(7).

During puberty, there is an increment in nipple (papilla) and nipple areola in both girls and boys, but especially in the earlier. The increment in nipple diameter is greater during stages B4 and B5, which helps to differentiate stages B3, 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 x C(2) with V for volume, L for longitudinal diameter, and C for cross-sectional diameter.

The measurement of testicular volume by ultrasonography employs the same principle, though it has been reported as the most precise method(11). We were able to show, in a different article, that all methods offer comparable reliability as long as the volumes obtained are 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 method is, thus, simple and its reliability comparable to that of orchidometer and ultrasonography(12).

Figure 5 -
Scheme for graphic measurement of testicular volume. The testicle is palpated and visually compared with the graphic models. Testicular volume is determined according to one of the six volumes or one of the intermediate volumes between two consecutive volumes depicted . The entire measurement scale includes 13 volumes: less than 2ml, 2ml, 3.5ml, 5ml, 7.5ml, 10ml, 12.5ml, 15ml, 17.5ml, 20ml, 22.5ml, 25ml, and greater than 25ml

In general, the testes of children have one to two, and sometimes three, ml in volume. Testes with four ml or more are, almost as a rule, characteristic of puberty. Consequently, attaining a volume of four ml or more is an indication of G2; this is an example of how measurement of testicular volume can help to carry out pubertal staging. A testicular volume of three ml is generally prognostic of puberty, for an estimated 80% chance of starting within the following six months(7). Eleven to 12-year old boys with small testes (one to two ml) are probably affected by delay of pubertal development (usually constitutional).

Measuring testicular volume is also important for the assessment of diagnosis of certain pathologies; for example, cases of Klinefelter syndrome (small testes) or of Fragile-X syndrome (possible macro-orchidism). The follow-up measurement of testicular volume is important in postsurgical follow-up of orchipexy (to check whether ectopy, twisting and/or surgical handling has affected testicular development) or of varicocele (that presents risk for testicular hypertrophy and subfertility).

Most adolescents have similar left- and right-hand side testicular volumes; however, it is common for the left-hand side testicle to have a slightly lower volume than the right-hand side one. In cases of significant differences (20%), it is important to examine the patient for factors that may be interfering in growth of the smaller testis (varicocele, previous surgery, orchitis, twisting, etc).

Testicular volume is significantly correlated with the testicular function. Some authors consider a testicular volume of 12 ml, attained, in average, around 13 to 14 years of age and during maximum growth velocity, the minimum volume compatible with fertility; in this sense, attainment of this volume is comparable to menarche as a reference for male 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, for example, can vary from 12 to 30 ml in volume(7).