Symposium on Adolescent Medicine
Physical Growth and Development During Puberty H. Verdain Barnes, M.D.*
Pubertal growth and development is unique. A working knowledge of its onset, sequence, and characteristics are prerequisite to the provision of effective comprehensive medical care to the adolescent. Normally, this maturation process begins and ends during the second decade of life. The exact chronologic timing of the initiation, progression, and completion as well as the degree of linear growth, weight gain, and secondary sexual development are, however, variable from individual to individual and between the sexes. These somatic changes follow or parallel the distinctive hormonal changes of puberty. This article will focus on the critical features of the changes in body composition, linear growth, weight gain, and secondary sexual development and their normal variability.
CHANGES IN BODY COMPOSITION Lean and non-lean body mass, as measured by a variety of techniques, average a two-fold increase during puberty." Lean body mass, principally muscle mass, shows a steady increase from the onset of puberty to its completion. The velocity of accumulation of lean body mass begins a sharp rise in the male at an average height of about 137 cm and a less dramatic rise in the female at about 112 cm, as shown in Figure 1A.3. 12 Lean body mass is qualitatively and quantitatively greater in the male than the female, which in part explains the generally greater strength of the male than the female at comparable stages of overall pubertal development. Non-lean body mass, principally fat, likewise increases during puberty. In the 3 years preceding peak height velocity there is a modest decrease in the rate of fat accumulation in the female as compared to a rather dramatic decrease in the male, who usually shows an actual loss of fat at the time of peak height velocity. Once peak height velocity is "Formerly Director. Adolescent Medicine, and Assistant Professor of Medicine, Pediatrics, and Radiology, The lohns Hopkins Hospital; Presently Associate Professor of Medicine and Pediatrics, and Director of Adolescent Medicine, University of Iowa Hospitals and Clinics, Iowa City, Iowa Medical Clinics of North America- Vol. 59, No. 6, November 1975
1305
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CHRONOLOGIC AND BONE AGE
Figure 1. The mean changes in muscle mass, fat mass, height and weight as correlated to stage of pubertal development and mean chronologic age in normal males and females. PHV -peak height velocity. M-menarche. (Derived from references 3, 6, 7,9 and reproduced by permission of the authors and publishers.)
reached there is a dramatic increase in the velocity of fat accumulation in the female and to a lesser degree in the male as shown in Figure IBY By the time somatic maturation is complete, the average female has twice the amount of body fat as the male. The greater proportion of fat in the female may play a critical role in the onset and maintenance of menses. The studies of Frisch et al. 4 indicate that about 17 per cent of body composition as fat is probably needed for menarche to occur and about 22 per cent for the onset and maintenance of regular ovulatory periods. Skeletal mass and the size of the heart, lungs, liver, spleen, kidneys, pancreas, thyroid, adrenals, gonads, phallus, and uterus double during puberty. There is also a small but distinct increase in the size of the central nervous system. Only the thymus, tonsils, and adenoids show a measureable decrease in size.!
1307
PHYSICAL GROWTH AND DEVELOPMENT
GROWTH IN HEIGHT During puberty, both males and females achieve the final 20 to 25 per cent of their linear growth. The majority of this increase in height occurs during the adolescent growth spurt which spans a period of 24 to 36 months. The adolescent growth spurt (Figure le) is characterized by (1) a sharp acceleration in linear growth velocity as measured by the increment of height gain in centimeters over a full 12 month period, (2) a peak period of growth, peak height velocity, and (3) a sharp decline in the increment of yearly growth. In general, this spurt occurs about 2 years earlier and is somewhat less quantitatively in the female than in the male. The onset of the normal growth spurt is quite variable; it may begin as early as 9.5 years or as late as 14.5 years in the female, and in the male as early as 10.5 years or as late as 16.0 years. Cross-sectional studies of British adolescents by Tanner et al. show that the average mean chronologic age of the peak height velocity is 12.1 years for the female and 14.1 years for the male. 6 • 7.11 These and subsequent data in the British population are generally applicable to adolescents in the United States and other comparably nourished populations. The velocity of linear growth is variable, but for an individual the pattern of growth is steady and consistent along a given percentile showing only modest, if any, variability. The third, fiftieth, and ninetyseventh percentiles which have been derived from longitudinal studies of the yearly increments in linear growth in the year of the peak height velocity and the 3 years before and after, along with the corresponding average chronologic age, are shown in Table 1.10.11 For clinical purposes the third and ninety-seventh percentiles define the limits of normal Table 1.
Normal Limits for Linear Growth Velocity During Puberty':'
AVERAGE CHRONOLOGIC AGE
YEAR RELATIVE TO
PHV
(cm/12 mos) 50th
PERCENTILE
3rd
97th
MALES
11 12 13 14 15 16 17
2 3 PHV 5 6 7
9 10 11 12 13 14 15
1 2 3 PHV 5 6 7
3.6 3.4 4.4 7.2 3.6 1.0 0.0
5.0 4.9 6.4 9.4 5.8 2.6 1.0
6.2 6.4 8.0 11.8 8.0 4.4 2.0
5.4 5.4 6.6 8.3 5.2 2.2 0.7
6.9 7.0 8.4 10.4 7.4 4.0 l.7
FEMALES
PHV = Peak Height Velocity ':'Derived from Tanner et al.'()
4.0 3.8 4.6 6.2 3.4 0.6 0.0
H.
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VERDAIN BARNES
variability. The adolescent who falls beyond the third or ninety-seventh percentiles in the absence of a genetic predisposition to tall or short stature or who shows a deviation from his or her own growth pattern, requires an evaluation for the causes of abnormal growth excess or retardation (see article on Delayed Puberty).
WEIGHT GAIN Normally, about 50 per cent of ideal adult body weight is gained during puberty. The velocity of weight gain, like height, accelerates, peaks, peak weight velocity, and decelerates as shown in Figure ID. In timing, the yearly weight increment during puberty generally parallels that of height, but is relatively greater than height and has greater individual and group variability. The peak weight velocity in the female occurs about 6 months after peak height velocity while in the male peak height velocity and peak weight velocity are simultaneous; in the female, peak weight velocity precedes that of the male by about 1.5 years and is quantitatively less than in the male. The variability in weight gain velocity, as derived from the longitudinal studies of Tanner et al., are shown in Table 2. 10 • 11 The third, fiftieth, and ninety-seventh percentiles are given in kilograms per year for the 12 months of peak weight velocity and the 3 years before and after as well as the average chronologic age for each. Weight gain is continuous throughout puberty and is relatively consistent along a given percentile for each individual. The third and ninety-seventh percentiles
Table 2. AVERAGE CHRONOLOGIC AGE
Normal Limits for the Velocity of Weight Gain During Puberty':' YEAR RELATIVE
TOPWV
11 12 13 14 15 16 17
2 3 PWV 5 6 7
9.5 10.5 11.5 12.5 13.5 14.5 15.5
1 2 3 PWV 5 6 7
3rd MALES 1.4 1.6 2.8 6.1 3.3 0.4 0.0
PERCENTILE (kg/12 mos) 50th
97th
3.1 4.0 5.4 9.0 5.7 2.6 1.0
6.2 6.8 8.6 12.8 9.0 4.8 2.3
3.0 3.5 5.6 8.3 5.3 2.2 1.0
5.8 6.4 8.6 10.6 7.6 5.0 3.4
FEMALES
PWV = Peak Weight Velocity. :'Derived from Tanner et al lO
1.3 1.8 3.0 5.5 0.8 0.1 0.0
PHYSICAL GROWTH AND DEVELOPMENT
1309
define the limits of normal variability. Distinct changes in an individual's weight gain pattern or percentile merits careful evaluation. As a general rule, the individual height percentile and weight percentile should not differ by more than 15 percentile points for the chronologic age. For example, a 14 year old girl with a fiftieth percentile height and an eightieth percentile weight is tending toward obesity while if the same individual had a thirtieth percentile weight there is a question of the patient being inappropriately underweight. A plateauing or a decrease in weight during puberty may be the first manifestation of a developing chronic disease. These patients should be evaluated for inflammatory bowel disease, particularly regional enteritis, chronic infections such as tuberculosis, hyperthyroidism, diabetes mellitus, collagen vascular diseases such as systemic lupus erythematosus and juvenile rheumatoid arthritis, chronic liver disease, chronic renal disease, inappropriate voluntary caloric deprivation due to a pathologic fear of obesity or classic anorexia nervosa, or socioeconomic malnutrition. Conversely, the patient whose pubertal weight gain is well in excess of the simultaneous increment in linear growth or whose weight is 20 per cent or more over an ideal body weight for height at the onset of puberty should be evaluated for the potential causes of obesity. In our experience almost all such patients are en route to becoming or already are exogenously obese. Most have combination hypertropic-hyperplastic obesity and require careful counseling in nutrition and caloric intake (see article on Obesity).
MALE SECONDARY SEXUAL DEVELOPMENT Secondary sexual development in the male involves genital development and pubic hair growth. During puberty the testes, epididymides, and prostate show a seven-fold or greater increase in size.I ,8 The prepubertal testicle is 1.5 cc or less in size as compared to 20 cc or greater in the adult. The stretched flaccid penis measured from the mons veneris to the tip of the glans has an approximate median length of 6.2 cm in the prepubertal male as compared to 13.2 cm in the adult with the tenth percentile being 4.8 and 10.8 cm and the nintieth percentile 7.5 and 15.5 cm respectively. Genital and pubic hair changes progress in an orderly fashion but are not necessarily coincident with one another; therefore, in staging pubertal development, it is important to stage each parameter separately. The established and most useful criteria for staging secondary sexual development are those of Tanner.9 A modification of these criteria is shown in Table 3. All adolescents should have their pubertal development staged at each visit as a basis for reassuring patients that they are progressing normally or to spot early any developmental abnormalities. The age of onset of secondary sexual development, the duration between developmental stages, and the correlation between the stages of genital and pubic hair growth are variable. Normal variations must be appreciated if the staging criteria are to be used appropriately to assess a
BREAST
Prepubertal Budding-elevation above chest wall by mound of subareolar breast tissue Larger and more elevation Larger and more elevation
Adult (size variable)
B1 B2
B3 B4"""
B5
20 cc
1.6 cc 1.6-6 cc 6-12.5 cc 12.5-20 cc
TESTES SCROTUM
PHALLUS
Prepubertal Minimal or no enlargement Increased length Increased length, circumference and glans size Adult
Prepubertal Areola- widens Papilla-erect Areola-further widening Areola and papilla form a mound projecting from the breast contour No mound, areola and breast in same plane
AREOLA AND PAPILLA
FEMALE
Prepubertal Becomes reddened, thinner and larger Greater thinning and enlargement Color darkens and further enlargement Adult
MALE
Staging Criteria For Secondary Sexual Development"
BREAST STAGE
G5
G3 G4
G2
G1
GENITAL STAGE
Table 3.
..-
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Male-spread to mons veneris Female-increased area of mons veneris
Male - greater area of mons veneris Female-almost entire mons veneris
Male-entire mons veneris and Female-medial aspect of the thighs
Male-extension up Female-linea alba
PH3
PH4
PH5
PH6'"
Derived from Tanner (1962) and Lee et aL (1974), ''':'Does not occur in all individuals.
Male- Base of phallus and/or scrotum Female - Labia majora and/or mons veneris
PH2
++++
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++
++
+
+
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AMOUNT
MALE AND FEMALE
Male-O Female-O
DISTRIBUTION
PHI
PUBIC HAIR STAGE
Adult
Adult
Greater curl and coarseness
Increased curl, coarseness, and pigmentation
Long (straight or curly), slightly pigmented, and downy
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VERDAIN BARNES
Table 4. Means and Normal Variation in the Timing of Adolescent Secondary Sexual Development':'
STACE
MEAN AGE OF ONSET ±2 SD (yrs)
STAGE
G2 G3 PH2 G4 PH3 PH4 G5 PH5
11.6 ± 2.1 12.9 ± 2.1 13.4 ± 2.2 .... 13.8 ± 2.0 13.9±2.1 14.4 ± 2.2 14.9 ± 2.2 15.2 ± 2.1
MALES G2-3 PH2-3 G3-4 PH3-4 G4-5 PH4-5 G2-5 PH2-5
B2 PH2 B3 PH3 PH4 B4 PH5 B5
11.2 11.7 12.2 12.4 12.9 13.1 14.4 15.3
B2-3 PH2-3 B3-4 PH3-4 B4-5 PH4-5 B2-5 PH2-5
TIME BETWEEN STAGES (yrs) Percentile Mean 5th 95th
1.1 0.5 0.8 0.4 1.0 0.7 3.0 1.6
0.4 0.1 0.2 0.3 0.4 0.2 1.9 0.8
2.2 1.0 1.6 0.5 1.9 1.5 4.7 2.7
0.9 0.6 0.9 0.5 2.0 1.3 4.0 2.5
0.2 0.2 0.1 0.2 0.1 0.6 1.5 1.4
1.0 1.3 2.2 0.9 6.8 2.4 9.0 3.1
FEMALES ± ± ± ± ± ± ± ±
2.2 2.4 2.1 2.2 2.1 2.3 2.2 3.5
':'Derived from Marshal! and Tanner,,·7 '·.... Mean is probably too high due to experimental method.
patient's progress through puberty. A guide to acceptable normal variability is shown in Tables 4 and 5. Several developmental features and correlations are particularly pertinent to the assessing of appropriate pubertal growth and development. First, as shown in Table 4, the mean age of genital stage 2 is 11.6 years with a standard deviation of 1 year. Consequently, any patient achieving G2 prior to 9.5 years of age must be evaluated for the potential causes of precocious puberty and those not in stage G2 by 13.7 years of age require evaluation for the causes of delayed puberty (see article on delayed puberty). Second, in the average normal male secondary genital development will be completed by 14.9 years of age though it may occur as early as age 12.7 years or as late as 17.1 years. The progression from one stage to the next is also quite variable (Table 4); it may take some normal boys as long to progress from stage G2 to G3 as it takes others to pass from G2 to G5. Patients who require longer than 2.2 years to move from G2 to G3, 1.6 years to pass from G3 to G4, 1.9 years to progress from G4 to G5, or have not reached G5 by 17.1 years of age require evaluation for the potential causes of delayed puberty. Third, as shown in Table 5, it is rare for an individual to reach stage 2 of pubic hair growth while still in genital stage 1. Under these circumstances, a patient should be evaluated for possible hypothalamic, pituitary, or gonadal dysfunction. Fourth, about 75 per cent of normal males reach peak height and weight velocity while in stage G4 with only 2 per cent reaching peak height velocity prior to that time and
1313
PHYSICAL GROWTH AND DEVELOPMENT
Table 5.
Important Correlations Between Genital and Pubic Hair Stages':' MALES
2
Pubic Hair Stage
2 3 4 5
98 2 0 0 0
Per Cent in Genital Stages
72 17 9 2 0
3
4
5
16 37 36
0 0 8 54 38
0 0 0 10 90
3
4
5
22 28 33 16 1
4 10 24 51
0 2 7 35 56
11
0
FEMALES
2 2 3 4 5
79 16 3 2 0
61 29 8 2 0
Breast Stage
11
':'Derived from Marshal! and Tanner',·7
about a fifth experiencing peak height velocity after reaching G5. Only 5 per cent will not have achieved peak height velocity by the time pubic hair stage 5 is reached. 7 Consequently, males who have not reached G4, and are concerned about their lack of height and/or weight in comparison to peers, can be reassured that their growth spurt is yet to come. The rare individual who has reached genital and pubic hair stage 4 without a growth spurt should be evaluated for thyroid and growth hormone deficiency and occult chronic disease. Finally, the data in tables 4 and 5 provide a basis for making appropriate estimates in counseling adolescents and their parents about pubertal growth and development. Such discussions can be of immense psychological benefit to the boy and his parents who are concerned or distraught about the pubertal process. During puberty there is normally an increase in the size of the areola of the male breast. In addition, at least 30 per cent and perhaps more normal adolescent males will develop varying amounts of discrete breast tissue which is best termed benign adolescent gynecomastia. Adolescent gynecomastia is usually bilateral and non tender, but about 20 per cent have unilateral development and/or tenderness. In the majority, this gynecomastia develops rapidly over a period of 1 to 6 months during mid adolescence and then spontaneously recedes during the following 6 to 18 months. Gynecomastia that persists unchanged for a period of 24 months is unlikely to resolve and surgical correction should be undertaken if it is psychosocially disabling to the patient. Obviously, all the potential causes of pathologic gynecomastia must be considered in these patients, but it is rare to uncover another etiology. The growth of facial and axillary hair has even greater variability than that of pubic hair. In general axillary hair growth begins about 24 months after PH2 has been reached, though occasionally it precedes
1314
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VERDAIN BARNES
pubic hair. Facial hair usually begins during PH3 and reaches an adult distribution around the time G5 and PH5 are reached. The usual sequence of growth is (1) the appearance of dark pigmented hair at the corners of the upper lip, (2) then the entire upper lip, the cheeks, below the lower lip in the midline, and (3) finally over the chin. The breaking and deepening of the voice usually occurs in late adolescence at a time when serum testosterone levels have reached an adult level.
FEMALE SECONDARY SEXUAL DEVELOPMENT Secondary sexual development in the female involves the enlargement of the ovaries, uterus, vagina, labia, breasts, and growth of pubic hair. The first visible sign of puberty in the female is the appearance of breast budding and/or pubic hair growth. Breast and pubic hair growth follow an orderly sequence of development but do not necessarily coincide with one another; consequently, each parameter must be staged separately. The criteria for breast and pubic hair staging is based on the criteria of Tanner" and are outlined in Table 3. It is of note that breast stage 4 does not occur in about 20 per cent of normal females. The age at which secondary sexual development begins, the rate of progression from one stage to the next, and the correlations between breast stage and pubic hair stage are variable. In the female as in the male, it is important for the physician to have a working knowledge of the normal variation of these events in order to evaluate and counsel the adolescent girl appropriately. A guide to acceptable normal variability for each of these parameters is shown in Table 5. The following features of development and interdevelopmental correlations are of particular importance. First, the mean age for the beginning of breast development (stage B2) is 11.2 years and pubic hair growth (stage PH2) 11.7 years with a standard deviation of 1.1 and 1.2 years respectively.6 Classifying normal as the mean ± 2 SD, any patient with breast development before the age of 9 years should be evaluated for premature thelarche in the absence of associated pubic hair growth, and precocious puberty if pubic hair is also present. Those with pubic hair stage 2 before the age of 9.3 years should be evaluated for premature pubarche. Conversely, girls without stage 2 breasts by 13.4 years of age or pubic hair growth by 14.1 years should be evaluated for the causes of delayed puberty. Second, as shown in Table 4, the progression from one stage of development to another is quite variable. Some normal females require a longer period of time to move from breast stage 3 to 4 than some require to move from stage B2 to B5. Those girls who require longer than 1 year to move from stage B2 to B3, 2.2 years from B3 to B4, or 6.8 years from B4 to B5 should be evaluated for delayed puberty. Third, from Table 5, it is clear that a significant number of girls will have stage 2 pubic hair development before reaching stage 2 breast development. On the other hand, it is rare for a girl to reach pubic hair stage 3 or 4 without breast development. Such girls should be evaluated for the presence of hypo thalamic, pituitary, or gonadal dysfunction. If
PHYSICAL GROWTH AND DEVELOPMENT
1315
accompanied by short stature, a chromosomal analysis should be performed to rule out classic or mosaic gonadal dysgenesis. In the presence of otherwise normal growth and development with evidence of normal estrogenization, consideration should be given to a congenital absence of breast tissue or possible end organ insensitivity to estrogen. Fourth, approximately one-half of girls reach peak height velocity during stage B3 and about a quarter in each B2 and B4, while peak height velocity occurs about equally in pubic hair stages 2 and 3 with a few still in stage 1 and stage 4. These data as well as that in Tables 4 and 5 provide a basis for counseling of adolescent females and their parents about normal growth and development. Adolescent females are often concerned about breast size. There are no normal standards for size. The patient's height, weight, level of estrogen or progesterone once in the normal adult range, or breast size of other females in the family do not have a high correlation with amount of breast tissue, though overall breast size is to some degree influenced by weight. The vast majority of females achieve adult breast size between the ages of 11 and 19.
MENARCHE The onset, continuation, and regularity of menses are a major concern to adolescent females and their parents particularly the mother. The mean age of menarche in British females is 13.5 years of age 6 and 12.7 years for girls in the United States,l:l with a standard deviation of 1.0 and 1.2 years, respectively. Menarche occurs at about the time of maximum deceleration of linear growth following peak height velocity. This usually coincides or follows shortly after reaching peak weight velocity. The girl's weight, more precisely her total body fat, may play a critical role. Shown in Figure 1 by the solid line is the minimum weight in kilograms for a given height at which adequate body fat is present to expect menses to begin.4 There are so few exceptions that this graph can be used as a guide in evaluating girls with primary amenorrhea. Menses occurs in approximately 5 per cent of normal girls who are in breast stage B2, about 25 per cent in B3, close to 60 per cent in B4, and about 10 per cent in B5. 6 About 99 per cent of normal females have the onset of menses within 5 years of beginning breast development. 6 The adolescent female who has already achieved peak height velocity and adequate weight for height, and has evidence of secondary sexual development, but has not menstruated by 15.5 years of age and/or within 5 years of starting breast development should be fully evaluated for other possible causes of primary amenorrhea. On the other hand, girls who are greater than the third percentile in height and have not had their growth spurt, or whose weight is under that expected for the onset of menses, or are not beyond breast and pubic hair stage 4 or are not 5 years beyond the onset of breast development, need only supportive, watchful waiting, and careful follow up. Conversely, patients who begin menses prior to 10.3 years of age should be evaluated for the causes of precocious puberty.
1316
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I G H
46 44 42
T
40
(kg)
38 36 34 32 30/
/
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VERDAIN BARNES
56 54 52 50 48 46 44 42 40 38 36 34 32 30
28
28
~
~
125130135140145150155160165170175180 HEIGHT(cm)
Figure 2. The weight for height at which menarche is likely to occur (solid line) and the weight for height at which regular ovulatory menstrual periods are likely to be maintained (broken line). (From Frisch, R. F., and McArthur, J. W.: Science, 185:949,1974, reproduced with permission.)
Menses are usually irregular for several months before assuming a regular pattern. Menses become regular at a mean age of 13.8 years with a standard deviation of about two yearsP Consequently, there should be no major concern about irregular menses for the first 2 years after menarche. Such patients who are concerned can be reassured in this regard. Patients with irregular menses beyond 2 years post menarche should have a thorough gynecologic evaluation.
REFERENCES 1. Boyd, E.: In growth, including reproduction and morphological development. Fed. Am.
Soc. Exper. BioI., Washington, D.C., 1962. 2. Cheek, D. B.: Human Growth: Body Composition, Cell Growth, Energy, and Intelligence. Philadelphia, Lea and Febiger, 1968. 3. Cheek, D. B.: Body composition, hormones, nutrition and adolescent growth. In Grumbach, M. M., Grave, G. D., and Mayer, F. E., eds.: Control of the Onset of Puberty. New York, J. Wiley and Sons, 1974. 4. Frisch, R. E., and McArthur, J. W.: Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science, 185:949, 1974.
PHYSICAL GROWTH AND DEVELOPMENT
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5. Frisch, R. E.: Critical weight at menarche, initiation of the adolescent growth spurt, and control of puberty. In Grumbach, M. M., Grave, G. D., and Mayer, F. E., eds.: Control of the Onset of Puberty. New York, J. Wiley and Sons, 1974. 6. Marshall, W. A., and Tanner, J. M.: Variations in pattern of pubertal changes in girls. Arch. Dis. Child., 44:291,1969. 7. Marshall, W. A., and Tanner, J. M.: Variations in the pattern of pubertal changes in boys. Arch. Dis. Child., 45:13,1970. 8. Schonfeld, W. A., and Beebe, G. W.: Normal growth and variation in the male genitalia from birth to maturity. J. Urol.,48:759, 1942. 9. Tanner, J. M.: Growth at Adolescence. Oxford, Blackwell Scientific Publishers, 2nd ed., 1962. 10. Tanner, J. M., and Whitehouse, R. H.: Growth and development record. BHWV 13 and 14, 1966. 11. Tanner, J. M., Whitehouse, R. H., and Takaishi, M.: Standards from birth to maturity for height, weight, height velocity, weight velocity: British children, 1965. Part I and I!. Arch. Dis. Child., 41 :454, 613,1966. 12. Tanner, J. M.: Growth of bone, muscle, and fat during childhood and adolescence. In Lodge, M. E., ed.: Growth and Development of Mammals. Butterworths, London, 1968. 13. Zacharias, L., Wurtman, R. J., et al.: Sexual maturation in contemporary American girls. Amer. J. Obstet. Gynec., 108:833, 1970. University of Iowa Hospitals and Clinics Iowa City, Iowa 52242
Physical Growth and Development During Puberty H. Verdain Barnes, M.D.*
Pubertal growth and development is unique. A working knowledge of its onset, sequence, and characteristics are prerequisite to the provision of effective comprehensive medical care to the adolescent. Normally, this maturation process begins and ends during the second decade of life. The exact chronologic timing of the initiation, progression, and completion as well as the degree of linear growth, weight gain, and secondary sexual development are, however, variable from individual to individual and between the sexes. These somatic changes follow or parallel the distinctive hormonal changes of puberty. This article will focus on the critical features of the changes in body composition, linear growth, weight gain, and secondary sexual development and their normal variability.
CHANGES IN BODY COMPOSITION Lean and non-lean body mass, as measured by a variety of techniques, average a two-fold increase during puberty." Lean body mass, principally muscle mass, shows a steady increase from the onset of puberty to its completion. The velocity of accumulation of lean body mass begins a sharp rise in the male at an average height of about 137 cm and a less dramatic rise in the female at about 112 cm, as shown in Figure 1A.3. 12 Lean body mass is qualitatively and quantitatively greater in the male than the female, which in part explains the generally greater strength of the male than the female at comparable stages of overall pubertal development. Non-lean body mass, principally fat, likewise increases during puberty. In the 3 years preceding peak height velocity there is a modest decrease in the rate of fat accumulation in the female as compared to a rather dramatic decrease in the male, who usually shows an actual loss of fat at the time of peak height velocity. Once peak height velocity is "Formerly Director. Adolescent Medicine, and Assistant Professor of Medicine, Pediatrics, and Radiology, The lohns Hopkins Hospital; Presently Associate Professor of Medicine and Pediatrics, and Director of Adolescent Medicine, University of Iowa Hospitals and Clinics, Iowa City, Iowa Medical Clinics of North America- Vol. 59, No. 6, November 1975
1305
1306
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~PHV M 125 1 1 1 1 100 GAIN IN 75 1 /~ MUSCLE 50 "'~ MASS ---",---"'---1 UNITS 25
VERDAIN BARNES
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G-GENITAL 8-8REAST P-PU8IC HAIR
CHRONOLOGIC AND BONE AGE
Figure 1. The mean changes in muscle mass, fat mass, height and weight as correlated to stage of pubertal development and mean chronologic age in normal males and females. PHV -peak height velocity. M-menarche. (Derived from references 3, 6, 7,9 and reproduced by permission of the authors and publishers.)
reached there is a dramatic increase in the velocity of fat accumulation in the female and to a lesser degree in the male as shown in Figure IBY By the time somatic maturation is complete, the average female has twice the amount of body fat as the male. The greater proportion of fat in the female may play a critical role in the onset and maintenance of menses. The studies of Frisch et al. 4 indicate that about 17 per cent of body composition as fat is probably needed for menarche to occur and about 22 per cent for the onset and maintenance of regular ovulatory periods. Skeletal mass and the size of the heart, lungs, liver, spleen, kidneys, pancreas, thyroid, adrenals, gonads, phallus, and uterus double during puberty. There is also a small but distinct increase in the size of the central nervous system. Only the thymus, tonsils, and adenoids show a measureable decrease in size.!
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PHYSICAL GROWTH AND DEVELOPMENT
GROWTH IN HEIGHT During puberty, both males and females achieve the final 20 to 25 per cent of their linear growth. The majority of this increase in height occurs during the adolescent growth spurt which spans a period of 24 to 36 months. The adolescent growth spurt (Figure le) is characterized by (1) a sharp acceleration in linear growth velocity as measured by the increment of height gain in centimeters over a full 12 month period, (2) a peak period of growth, peak height velocity, and (3) a sharp decline in the increment of yearly growth. In general, this spurt occurs about 2 years earlier and is somewhat less quantitatively in the female than in the male. The onset of the normal growth spurt is quite variable; it may begin as early as 9.5 years or as late as 14.5 years in the female, and in the male as early as 10.5 years or as late as 16.0 years. Cross-sectional studies of British adolescents by Tanner et al. show that the average mean chronologic age of the peak height velocity is 12.1 years for the female and 14.1 years for the male. 6 • 7.11 These and subsequent data in the British population are generally applicable to adolescents in the United States and other comparably nourished populations. The velocity of linear growth is variable, but for an individual the pattern of growth is steady and consistent along a given percentile showing only modest, if any, variability. The third, fiftieth, and ninetyseventh percentiles which have been derived from longitudinal studies of the yearly increments in linear growth in the year of the peak height velocity and the 3 years before and after, along with the corresponding average chronologic age, are shown in Table 1.10.11 For clinical purposes the third and ninety-seventh percentiles define the limits of normal Table 1.
Normal Limits for Linear Growth Velocity During Puberty':'
AVERAGE CHRONOLOGIC AGE
YEAR RELATIVE TO
PHV
(cm/12 mos) 50th
PERCENTILE
3rd
97th
MALES
11 12 13 14 15 16 17
2 3 PHV 5 6 7
9 10 11 12 13 14 15
1 2 3 PHV 5 6 7
3.6 3.4 4.4 7.2 3.6 1.0 0.0
5.0 4.9 6.4 9.4 5.8 2.6 1.0
6.2 6.4 8.0 11.8 8.0 4.4 2.0
5.4 5.4 6.6 8.3 5.2 2.2 0.7
6.9 7.0 8.4 10.4 7.4 4.0 l.7
FEMALES
PHV = Peak Height Velocity ':'Derived from Tanner et al.'()
4.0 3.8 4.6 6.2 3.4 0.6 0.0
H.
1308
VERDAIN BARNES
variability. The adolescent who falls beyond the third or ninety-seventh percentiles in the absence of a genetic predisposition to tall or short stature or who shows a deviation from his or her own growth pattern, requires an evaluation for the causes of abnormal growth excess or retardation (see article on Delayed Puberty).
WEIGHT GAIN Normally, about 50 per cent of ideal adult body weight is gained during puberty. The velocity of weight gain, like height, accelerates, peaks, peak weight velocity, and decelerates as shown in Figure ID. In timing, the yearly weight increment during puberty generally parallels that of height, but is relatively greater than height and has greater individual and group variability. The peak weight velocity in the female occurs about 6 months after peak height velocity while in the male peak height velocity and peak weight velocity are simultaneous; in the female, peak weight velocity precedes that of the male by about 1.5 years and is quantitatively less than in the male. The variability in weight gain velocity, as derived from the longitudinal studies of Tanner et al., are shown in Table 2. 10 • 11 The third, fiftieth, and ninety-seventh percentiles are given in kilograms per year for the 12 months of peak weight velocity and the 3 years before and after as well as the average chronologic age for each. Weight gain is continuous throughout puberty and is relatively consistent along a given percentile for each individual. The third and ninety-seventh percentiles
Table 2. AVERAGE CHRONOLOGIC AGE
Normal Limits for the Velocity of Weight Gain During Puberty':' YEAR RELATIVE
TOPWV
11 12 13 14 15 16 17
2 3 PWV 5 6 7
9.5 10.5 11.5 12.5 13.5 14.5 15.5
1 2 3 PWV 5 6 7
3rd MALES 1.4 1.6 2.8 6.1 3.3 0.4 0.0
PERCENTILE (kg/12 mos) 50th
97th
3.1 4.0 5.4 9.0 5.7 2.6 1.0
6.2 6.8 8.6 12.8 9.0 4.8 2.3
3.0 3.5 5.6 8.3 5.3 2.2 1.0
5.8 6.4 8.6 10.6 7.6 5.0 3.4
FEMALES
PWV = Peak Weight Velocity. :'Derived from Tanner et al lO
1.3 1.8 3.0 5.5 0.8 0.1 0.0
PHYSICAL GROWTH AND DEVELOPMENT
1309
define the limits of normal variability. Distinct changes in an individual's weight gain pattern or percentile merits careful evaluation. As a general rule, the individual height percentile and weight percentile should not differ by more than 15 percentile points for the chronologic age. For example, a 14 year old girl with a fiftieth percentile height and an eightieth percentile weight is tending toward obesity while if the same individual had a thirtieth percentile weight there is a question of the patient being inappropriately underweight. A plateauing or a decrease in weight during puberty may be the first manifestation of a developing chronic disease. These patients should be evaluated for inflammatory bowel disease, particularly regional enteritis, chronic infections such as tuberculosis, hyperthyroidism, diabetes mellitus, collagen vascular diseases such as systemic lupus erythematosus and juvenile rheumatoid arthritis, chronic liver disease, chronic renal disease, inappropriate voluntary caloric deprivation due to a pathologic fear of obesity or classic anorexia nervosa, or socioeconomic malnutrition. Conversely, the patient whose pubertal weight gain is well in excess of the simultaneous increment in linear growth or whose weight is 20 per cent or more over an ideal body weight for height at the onset of puberty should be evaluated for the potential causes of obesity. In our experience almost all such patients are en route to becoming or already are exogenously obese. Most have combination hypertropic-hyperplastic obesity and require careful counseling in nutrition and caloric intake (see article on Obesity).
MALE SECONDARY SEXUAL DEVELOPMENT Secondary sexual development in the male involves genital development and pubic hair growth. During puberty the testes, epididymides, and prostate show a seven-fold or greater increase in size.I ,8 The prepubertal testicle is 1.5 cc or less in size as compared to 20 cc or greater in the adult. The stretched flaccid penis measured from the mons veneris to the tip of the glans has an approximate median length of 6.2 cm in the prepubertal male as compared to 13.2 cm in the adult with the tenth percentile being 4.8 and 10.8 cm and the nintieth percentile 7.5 and 15.5 cm respectively. Genital and pubic hair changes progress in an orderly fashion but are not necessarily coincident with one another; therefore, in staging pubertal development, it is important to stage each parameter separately. The established and most useful criteria for staging secondary sexual development are those of Tanner.9 A modification of these criteria is shown in Table 3. All adolescents should have their pubertal development staged at each visit as a basis for reassuring patients that they are progressing normally or to spot early any developmental abnormalities. The age of onset of secondary sexual development, the duration between developmental stages, and the correlation between the stages of genital and pubic hair growth are variable. Normal variations must be appreciated if the staging criteria are to be used appropriately to assess a
BREAST
Prepubertal Budding-elevation above chest wall by mound of subareolar breast tissue Larger and more elevation Larger and more elevation
Adult (size variable)
B1 B2
B3 B4"""
B5
20 cc
1.6 cc 1.6-6 cc 6-12.5 cc 12.5-20 cc
TESTES SCROTUM
PHALLUS
Prepubertal Minimal or no enlargement Increased length Increased length, circumference and glans size Adult
Prepubertal Areola- widens Papilla-erect Areola-further widening Areola and papilla form a mound projecting from the breast contour No mound, areola and breast in same plane
AREOLA AND PAPILLA
FEMALE
Prepubertal Becomes reddened, thinner and larger Greater thinning and enlargement Color darkens and further enlargement Adult
MALE
Staging Criteria For Secondary Sexual Development"
BREAST STAGE
G5
G3 G4
G2
G1
GENITAL STAGE
Table 3.
..-
t"j Ul
Z
> ~
tJj
Z
o >
~
-< t"j
:::r:
o
..-
(.>Q
Male-spread to mons veneris Female-increased area of mons veneris
Male - greater area of mons veneris Female-almost entire mons veneris
Male-entire mons veneris and Female-medial aspect of the thighs
Male-extension up Female-linea alba
PH3
PH4
PH5
PH6'"
Derived from Tanner (1962) and Lee et aL (1974), ''':'Does not occur in all individuals.
Male- Base of phallus and/or scrotum Female - Labia majora and/or mons veneris
PH2
++++
++++
+++ +++
++
++
+
+
o o
AMOUNT
MALE AND FEMALE
Male-O Female-O
DISTRIBUTION
PHI
PUBIC HAIR STAGE
Adult
Adult
Greater curl and coarseness
Increased curl, coarseness, and pigmentation
Long (straight or curly), slightly pigmented, and downy
o o
TYPE
~
"1:1
..... I.>:l ..... .....
>-l
Z
OJ
;::
'tI
o
t'"
OJ
-l
o ::,;
::0
Cl
t'"
;..
>< rJl (l
1312
H.
VERDAIN BARNES
Table 4. Means and Normal Variation in the Timing of Adolescent Secondary Sexual Development':'
STACE
MEAN AGE OF ONSET ±2 SD (yrs)
STAGE
G2 G3 PH2 G4 PH3 PH4 G5 PH5
11.6 ± 2.1 12.9 ± 2.1 13.4 ± 2.2 .... 13.8 ± 2.0 13.9±2.1 14.4 ± 2.2 14.9 ± 2.2 15.2 ± 2.1
MALES G2-3 PH2-3 G3-4 PH3-4 G4-5 PH4-5 G2-5 PH2-5
B2 PH2 B3 PH3 PH4 B4 PH5 B5
11.2 11.7 12.2 12.4 12.9 13.1 14.4 15.3
B2-3 PH2-3 B3-4 PH3-4 B4-5 PH4-5 B2-5 PH2-5
TIME BETWEEN STAGES (yrs) Percentile Mean 5th 95th
1.1 0.5 0.8 0.4 1.0 0.7 3.0 1.6
0.4 0.1 0.2 0.3 0.4 0.2 1.9 0.8
2.2 1.0 1.6 0.5 1.9 1.5 4.7 2.7
0.9 0.6 0.9 0.5 2.0 1.3 4.0 2.5
0.2 0.2 0.1 0.2 0.1 0.6 1.5 1.4
1.0 1.3 2.2 0.9 6.8 2.4 9.0 3.1
FEMALES ± ± ± ± ± ± ± ±
2.2 2.4 2.1 2.2 2.1 2.3 2.2 3.5
':'Derived from Marshal! and Tanner,,·7 '·.... Mean is probably too high due to experimental method.
patient's progress through puberty. A guide to acceptable normal variability is shown in Tables 4 and 5. Several developmental features and correlations are particularly pertinent to the assessing of appropriate pubertal growth and development. First, as shown in Table 4, the mean age of genital stage 2 is 11.6 years with a standard deviation of 1 year. Consequently, any patient achieving G2 prior to 9.5 years of age must be evaluated for the potential causes of precocious puberty and those not in stage G2 by 13.7 years of age require evaluation for the causes of delayed puberty (see article on delayed puberty). Second, in the average normal male secondary genital development will be completed by 14.9 years of age though it may occur as early as age 12.7 years or as late as 17.1 years. The progression from one stage to the next is also quite variable (Table 4); it may take some normal boys as long to progress from stage G2 to G3 as it takes others to pass from G2 to G5. Patients who require longer than 2.2 years to move from G2 to G3, 1.6 years to pass from G3 to G4, 1.9 years to progress from G4 to G5, or have not reached G5 by 17.1 years of age require evaluation for the potential causes of delayed puberty. Third, as shown in Table 5, it is rare for an individual to reach stage 2 of pubic hair growth while still in genital stage 1. Under these circumstances, a patient should be evaluated for possible hypothalamic, pituitary, or gonadal dysfunction. Fourth, about 75 per cent of normal males reach peak height and weight velocity while in stage G4 with only 2 per cent reaching peak height velocity prior to that time and
1313
PHYSICAL GROWTH AND DEVELOPMENT
Table 5.
Important Correlations Between Genital and Pubic Hair Stages':' MALES
2
Pubic Hair Stage
2 3 4 5
98 2 0 0 0
Per Cent in Genital Stages
72 17 9 2 0
3
4
5
16 37 36
0 0 8 54 38
0 0 0 10 90
3
4
5
22 28 33 16 1
4 10 24 51
0 2 7 35 56
11
0
FEMALES
2 2 3 4 5
79 16 3 2 0
61 29 8 2 0
Breast Stage
11
':'Derived from Marshal! and Tanner',·7
about a fifth experiencing peak height velocity after reaching G5. Only 5 per cent will not have achieved peak height velocity by the time pubic hair stage 5 is reached. 7 Consequently, males who have not reached G4, and are concerned about their lack of height and/or weight in comparison to peers, can be reassured that their growth spurt is yet to come. The rare individual who has reached genital and pubic hair stage 4 without a growth spurt should be evaluated for thyroid and growth hormone deficiency and occult chronic disease. Finally, the data in tables 4 and 5 provide a basis for making appropriate estimates in counseling adolescents and their parents about pubertal growth and development. Such discussions can be of immense psychological benefit to the boy and his parents who are concerned or distraught about the pubertal process. During puberty there is normally an increase in the size of the areola of the male breast. In addition, at least 30 per cent and perhaps more normal adolescent males will develop varying amounts of discrete breast tissue which is best termed benign adolescent gynecomastia. Adolescent gynecomastia is usually bilateral and non tender, but about 20 per cent have unilateral development and/or tenderness. In the majority, this gynecomastia develops rapidly over a period of 1 to 6 months during mid adolescence and then spontaneously recedes during the following 6 to 18 months. Gynecomastia that persists unchanged for a period of 24 months is unlikely to resolve and surgical correction should be undertaken if it is psychosocially disabling to the patient. Obviously, all the potential causes of pathologic gynecomastia must be considered in these patients, but it is rare to uncover another etiology. The growth of facial and axillary hair has even greater variability than that of pubic hair. In general axillary hair growth begins about 24 months after PH2 has been reached, though occasionally it precedes
1314
H.
VERDAIN BARNES
pubic hair. Facial hair usually begins during PH3 and reaches an adult distribution around the time G5 and PH5 are reached. The usual sequence of growth is (1) the appearance of dark pigmented hair at the corners of the upper lip, (2) then the entire upper lip, the cheeks, below the lower lip in the midline, and (3) finally over the chin. The breaking and deepening of the voice usually occurs in late adolescence at a time when serum testosterone levels have reached an adult level.
FEMALE SECONDARY SEXUAL DEVELOPMENT Secondary sexual development in the female involves the enlargement of the ovaries, uterus, vagina, labia, breasts, and growth of pubic hair. The first visible sign of puberty in the female is the appearance of breast budding and/or pubic hair growth. Breast and pubic hair growth follow an orderly sequence of development but do not necessarily coincide with one another; consequently, each parameter must be staged separately. The criteria for breast and pubic hair staging is based on the criteria of Tanner" and are outlined in Table 3. It is of note that breast stage 4 does not occur in about 20 per cent of normal females. The age at which secondary sexual development begins, the rate of progression from one stage to the next, and the correlations between breast stage and pubic hair stage are variable. In the female as in the male, it is important for the physician to have a working knowledge of the normal variation of these events in order to evaluate and counsel the adolescent girl appropriately. A guide to acceptable normal variability for each of these parameters is shown in Table 5. The following features of development and interdevelopmental correlations are of particular importance. First, the mean age for the beginning of breast development (stage B2) is 11.2 years and pubic hair growth (stage PH2) 11.7 years with a standard deviation of 1.1 and 1.2 years respectively.6 Classifying normal as the mean ± 2 SD, any patient with breast development before the age of 9 years should be evaluated for premature thelarche in the absence of associated pubic hair growth, and precocious puberty if pubic hair is also present. Those with pubic hair stage 2 before the age of 9.3 years should be evaluated for premature pubarche. Conversely, girls without stage 2 breasts by 13.4 years of age or pubic hair growth by 14.1 years should be evaluated for the causes of delayed puberty. Second, as shown in Table 4, the progression from one stage of development to another is quite variable. Some normal females require a longer period of time to move from breast stage 3 to 4 than some require to move from stage B2 to B5. Those girls who require longer than 1 year to move from stage B2 to B3, 2.2 years from B3 to B4, or 6.8 years from B4 to B5 should be evaluated for delayed puberty. Third, from Table 5, it is clear that a significant number of girls will have stage 2 pubic hair development before reaching stage 2 breast development. On the other hand, it is rare for a girl to reach pubic hair stage 3 or 4 without breast development. Such girls should be evaluated for the presence of hypo thalamic, pituitary, or gonadal dysfunction. If
PHYSICAL GROWTH AND DEVELOPMENT
1315
accompanied by short stature, a chromosomal analysis should be performed to rule out classic or mosaic gonadal dysgenesis. In the presence of otherwise normal growth and development with evidence of normal estrogenization, consideration should be given to a congenital absence of breast tissue or possible end organ insensitivity to estrogen. Fourth, approximately one-half of girls reach peak height velocity during stage B3 and about a quarter in each B2 and B4, while peak height velocity occurs about equally in pubic hair stages 2 and 3 with a few still in stage 1 and stage 4. These data as well as that in Tables 4 and 5 provide a basis for counseling of adolescent females and their parents about normal growth and development. Adolescent females are often concerned about breast size. There are no normal standards for size. The patient's height, weight, level of estrogen or progesterone once in the normal adult range, or breast size of other females in the family do not have a high correlation with amount of breast tissue, though overall breast size is to some degree influenced by weight. The vast majority of females achieve adult breast size between the ages of 11 and 19.
MENARCHE The onset, continuation, and regularity of menses are a major concern to adolescent females and their parents particularly the mother. The mean age of menarche in British females is 13.5 years of age 6 and 12.7 years for girls in the United States,l:l with a standard deviation of 1.0 and 1.2 years, respectively. Menarche occurs at about the time of maximum deceleration of linear growth following peak height velocity. This usually coincides or follows shortly after reaching peak weight velocity. The girl's weight, more precisely her total body fat, may play a critical role. Shown in Figure 1 by the solid line is the minimum weight in kilograms for a given height at which adequate body fat is present to expect menses to begin.4 There are so few exceptions that this graph can be used as a guide in evaluating girls with primary amenorrhea. Menses occurs in approximately 5 per cent of normal girls who are in breast stage B2, about 25 per cent in B3, close to 60 per cent in B4, and about 10 per cent in B5. 6 About 99 per cent of normal females have the onset of menses within 5 years of beginning breast development. 6 The adolescent female who has already achieved peak height velocity and adequate weight for height, and has evidence of secondary sexual development, but has not menstruated by 15.5 years of age and/or within 5 years of starting breast development should be fully evaluated for other possible causes of primary amenorrhea. On the other hand, girls who are greater than the third percentile in height and have not had their growth spurt, or whose weight is under that expected for the onset of menses, or are not beyond breast and pubic hair stage 4 or are not 5 years beyond the onset of breast development, need only supportive, watchful waiting, and careful follow up. Conversely, patients who begin menses prior to 10.3 years of age should be evaluated for the causes of precocious puberty.
1316
H.
54 52 50 48
W E
I G H
46 44 42
T
40
(kg)
38 36 34 32 30/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
/
VERDAIN BARNES
56 54 52 50 48 46 44 42 40 38 36 34 32 30
28
28
~
~
125130135140145150155160165170175180 HEIGHT(cm)
Figure 2. The weight for height at which menarche is likely to occur (solid line) and the weight for height at which regular ovulatory menstrual periods are likely to be maintained (broken line). (From Frisch, R. F., and McArthur, J. W.: Science, 185:949,1974, reproduced with permission.)
Menses are usually irregular for several months before assuming a regular pattern. Menses become regular at a mean age of 13.8 years with a standard deviation of about two yearsP Consequently, there should be no major concern about irregular menses for the first 2 years after menarche. Such patients who are concerned can be reassured in this regard. Patients with irregular menses beyond 2 years post menarche should have a thorough gynecologic evaluation.
REFERENCES 1. Boyd, E.: In growth, including reproduction and morphological development. Fed. Am.
Soc. Exper. BioI., Washington, D.C., 1962. 2. Cheek, D. B.: Human Growth: Body Composition, Cell Growth, Energy, and Intelligence. Philadelphia, Lea and Febiger, 1968. 3. Cheek, D. B.: Body composition, hormones, nutrition and adolescent growth. In Grumbach, M. M., Grave, G. D., and Mayer, F. E., eds.: Control of the Onset of Puberty. New York, J. Wiley and Sons, 1974. 4. Frisch, R. E., and McArthur, J. W.: Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science, 185:949, 1974.
PHYSICAL GROWTH AND DEVELOPMENT
1317
5. Frisch, R. E.: Critical weight at menarche, initiation of the adolescent growth spurt, and control of puberty. In Grumbach, M. M., Grave, G. D., and Mayer, F. E., eds.: Control of the Onset of Puberty. New York, J. Wiley and Sons, 1974. 6. Marshall, W. A., and Tanner, J. M.: Variations in pattern of pubertal changes in girls. Arch. Dis. Child., 44:291,1969. 7. Marshall, W. A., and Tanner, J. M.: Variations in the pattern of pubertal changes in boys. Arch. Dis. Child., 45:13,1970. 8. Schonfeld, W. A., and Beebe, G. W.: Normal growth and variation in the male genitalia from birth to maturity. J. Urol.,48:759, 1942. 9. Tanner, J. M.: Growth at Adolescence. Oxford, Blackwell Scientific Publishers, 2nd ed., 1962. 10. Tanner, J. M., and Whitehouse, R. H.: Growth and development record. BHWV 13 and 14, 1966. 11. Tanner, J. M., Whitehouse, R. H., and Takaishi, M.: Standards from birth to maturity for height, weight, height velocity, weight velocity: British children, 1965. Part I and I!. Arch. Dis. Child., 41 :454, 613,1966. 12. Tanner, J. M.: Growth of bone, muscle, and fat during childhood and adolescence. In Lodge, M. E., ed.: Growth and Development of Mammals. Butterworths, London, 1968. 13. Zacharias, L., Wurtman, R. J., et al.: Sexual maturation in contemporary American girls. Amer. J. Obstet. Gynec., 108:833, 1970. University of Iowa Hospitals and Clinics Iowa City, Iowa 52242
