Bava Basra 155b ~ Delayed Puberty in Boys

In today's page of Talmud we read about the treatment for the delayed onset of puberty:

כי אתו לקמיה דרבי חייא אי כחוש אמר להו זילו אבריוהו ואי בריא אמר להו זילו אכחשוהו דהני סימנין זמנין דנתרי מחמת כחישותא וזמנין דנתרי מחמת בריותא

Whenever people came to Rabbi Hiyya [with a case of a man who had not developed pubic hair]  he would tell them, if [the man was] thin, ‘Let him gain weight’; and if they were overweight he would say ‘Go lose weight’; for these signs [of sexual maturity] are sometimes delayed as a result of emaciation and sometimes  as a result of obesity.   (Yevamot 97a)

Rabbi Hiyya probably lived in the second half of the second century, and the treatment he suggested is one of the earliest examples associating nutritional status and delayed puberty.  Elsewhere in the Talmud we find this statement attributed to Rava, who died around 350 CE. But whoever suggested it first, I have found nothing in the works of Hippocrates, Aristotle and Galen that address this issue, so this association does not appear to have been a widely held belief in antiquity that was simply being echoed in the Talmud. 

There has been some discussion of what appears to be the increasingly earlier onset of puberty in girls. In fact, menarche, (the age of a girl's first menstrual period) has been steadily decreasing by a consistent three years per century of record keeping. However, R. Hiyya was addressing not the early onset of puberty in girls, but its delayed appearance in boys.  He noted that this delay was sometimes related to extremes of nutritional status, and so in these cases, was amenable to intervention.

“R.Hiyya may have been the first first to report an association of obesity and delayed puberty in boys.”

R.Hiyya was on to something. He (or Rava) may in fact have been the first to report an association between obesity and delayed puberty in boys.  This association has been confirmed by several studies which found that obesity has different effects on puberty in boys and girls. In girls, obesity is associated with earlier puberty, while in boys it has the opposite effect, and delays sexual maturation. But it was not until 2010 this association was confirmed by a longitudinal population-based study. This reported that a "higher BMI z score trajectory" (i.e. obesity)  during early to middle childhood may be associated with later onset of puberty among boys. 

The finding that puberty may be delayed in boys who are underweight has also been confirmed. As far as I can tell, none of the researchers has credited Rava (who died around 350 CE.) or Rabbi Hiyya for being the first to notice these associations. But they were first, and firsts count for something in science.

Kiddushin 16b ~ Measuring Puberty

קידושין טז, ב

בן תשע שנים שהביא שתי שערות שומא מבן ט' שנים ויום אחד עד בן י"ב שנה ויום אחד ועודן בו שומא ר' יוסי בר' יהודה אומר סימן בן י"ג שנה ויום אחד דברי הכל סימן 

If a nine year old grows two hairs [in the pubic region] the growth should be attributed to a mole [and not as a sign of sexual maturity]. [If these hairs grow] from the age of nine years and one day until twelve years and one day, and they are still there [when the child reaches twelve, one opinion is that they should be attributed to a] mole, and Rabbi Yossi bar Rabbi Yehuda says they are a sign of sexual maturity. [If these hairs grow] when the child is thirteen years old and one day, then everyone agrees they are a sign of sexual maturity...(Kiddushin 16b)

Pre-Modern Descriptions of Puberty

The way in which children develop into adults has fascinated us for centuries.  In fact, the earliest surviving statement on human growth dates back to the sixth century BCE, (not long after the prophet Jeremiah lived) and is by the Athenian poet Solon. One critic described his poem as combining "scientific sense with philosophical probability (if not, regrettably, with poetic elegance)." Here is Solon:

A young boy acquires his first ring of teeth as an infant and sheds them before he reaches the age of seven years. When the god brings to an end the next seven year period, the boy shows the signs of beginning puberty. In the third hebdomad, [ a period of seven years] the body enlarges, the chin becomes bearded and the bloom of the boy's complexion is lost. In the forth hebdomad physical strength is at its peak and is regarded as the criterion of manliness; in the fifth hebdomad a man should take thought of marriage and seek sons to succeed him. In the sixth hebdomad a man's mind is in all things disciplined by experience and he no longer feels the impulse to uncontrolled behavior. In the seventh he is at his prime in mind and tongue and also in the eighth, the two together making fourteen years. In the ninth hebdomad, though he still retains some strength, he is too feeble in mind and speech for the greatest excellence. If a man continues to the end of the tenth hebdomad, he has not encountered death before due time.

Hippocrates believed that puberty could be delayed in areas where "the wind is cold and the water is hard". Rabbi Shimon ben Gamliel (d. 70CE) would have agreed, because he thought that the growth of pubic hair was hastened in those who used the bathhouse regularly.  But it is especially interesting to compare Aristotle's writings on puberty with those of the Talmud (which of course were codified several hundred years later).

In man, maturity is indicated by a change in the tone of the voice, by an increase in size and an alteration in appearance of the sexual organs, and also by an increase in size and alteration in appearance of breasts, and above in the hair growth above the pubes.

Aristotle (d. 322 BCE) seems to have put a lot of weight on the growth of pubic hair, just like the rabbis of  in the Talmud did many years later. Galen, who died in 199 CE, was cautious about timing the onset of puberty: "Some begin puberty at once on the completion of the fourteenth year, but some begin a year or more after that" (De Sanitate Tuenda, or p288 of this translation). Jumping forward several centuries, we find that girls in Tuscany in 1428 were allowed to marry aged eleven and a half, although they were forbidden to live with their husbands until they were twelve. However the Bishop of Florence (later canonized as Saint Anthony) declared that cohabitation was allowed "provided the girl had reached puberty." 

The Tanner Scale

Today, the stage of sexual maturity in children is most commonly measured using the Tanner scale, described by the British pediatrician James Tanner, who died in 2010.  (He wrote a fascinating History of the Study of Human Growth as a sort of a hobby, but his day job was working as a Professor at the Institute of Child  Health in London.)  Here is how Tanner described his scale in boys, (from his original paper published in 1970):

Stage 1: Pre-adolescent. The velus [sic] over the pubes is no further developed than that over the abdominal wall, i.e. no pubic hair.

Stage 2: Sparse growth of long, slightly pigmented downy hair, straight or slightly curled, appearing chiefly at the base of the penis. This stage is difficult to see on photographs, particularly of fair-headed subjects...

Stage 3: Considerably darker, coarser, and more curled. The hair spreads sparsely over the junction of the pubes. This and subsequent stages were clearly recognizable on the photographs.

Stage 4: Hair is now adult in type, but the area covered by it is still considerably smaller than in most adults. There is no spread to the medial surface of the thighs.

Stage 5: Adult in quantity and type, distributed as an inverse triangle of the classically feminine pattern. Spread to the medial surface of the thighs but not up the linea alba or elsewhere above the base of the inverse triangle.

“There has been less discussion in the literature as to whether the appearance of pubic hair has advanced in females, although this does seem to be the case, pubarche having advanced by at least 6 months. The PROS study found stage II pubic hair to be apparent in African-American females at a mean age of 8·78 years and 10·51 years in whites.”

— Slyper, AH.The pubertal timing controversy in the USA, and a review of possible causative factors for the advance in timing of onset of puberty. Clinical Endocrinology (2006) 65, 1–8

Tanner also described other signs of sexual maturity, since growth of pubic hair is not the only maker.  In boys, for example, Tanner used a five-stage system for genital growth: in stage one, the  "testes, scrotum, and penis are of about the same size and proportion as in early childhood," whereas in stage two, "the scrotum and testes have enlarged and there is a change in the texture of the scrotal skin..."  Tanner noted that the stages of pubic hair development and the stages of genital development differ, so that a boy may reach full genital maturation sooner than he reaches stage five on the pubic hair scale.  

From Marshall A. Tanner JM. Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood 1970. 45: 13-25.

Tanner's work reveals what we already know intuitively. Maturity, whether sexual or emotional, is a process that takes time and proceeds through many stages. The rabbis of the Talmud relied predominantly on one marker of adulthood:  sexual maturity as evidenced by a minimal of pubic hair growth.  But they used it in conjunction with the age of the child.  They also understood that the onset of these signs might be sooner in some children and later in others.

Sequence of events in puberty in girls (top) and boys. From Marshall A. Tanner JM. Variations in the pattern of pubertal changes in boys. Archives of Disease in Childhood 1970. 45:22.

In most European countries, the age of the onset of puberty (as measured by the onset of menstruation) has fallen by about a year per century. Boys also seem to be developing earlier than previously, possibly by more than a year. Data from the US National Health and Nutrition Examination Survey (NHANES III) study of boys aged 8 –19 years, suggests that the mean age of onset of male genital development based on visual inspection is now about nine years for African-Americans and ten years for white boys.

Another First?

Last year we analyzed talmudic statements of R. Hiyya (who lived in the second half of the second century,) and Rava, (d. 350CE) who appear to have been the first to report an association between obesity and delayed puberty in boys.  They claimed that puberty may be delayed in boys who are underweight, and this association has now been confirmed. As we noted then, none of the researchers has credited these talmudic sages for being the first to notice these associations. But Rava and R. Hiyya were first, and firsts count for something in science. The Baraita in today's daf  may be the first recorded discussion of the lower limits of sexual maturity. But the rabbis of the Talmud used other markers of maturity, like breast development which is discussed in Masechet Niddah (47a).They distinguished between "lower" and "upper" signs of puberty, and so presaged the work of Tanner. (The rabbis also ruled that "all girls who are examined are examined by women". Thank heavens.)

There were several reasons why the Talmud had to codify the stages of physical maturity.  Among these were to allow a father to decide to whom his daughter would marry.

A father who declares...my daughter is twelve years and a day is believed in order to marry the child off...(רמב׳ם הל׳ אישות ב:כג)

Today, any notion that a child under the age of twelve (or sixteen for that matter) would be mature enough to marry is utterly repugnant to us. But according to the UN in developing countries, one in every three girls is married before reaching the age of eighteen, and one in nine is married by the age of fifteen.  When we read the Talmud we often get a glimpse into a Jewish world very different from our own. But some practices of that world still exist outside of the Jewish community today, to the shame of us all. 

From United Nations Children’s Fund, Ending Child Marriage: Progress and prospects, UNICEF, New York, 2014.

Yevamot 97a ~ Rava on Delayed Puberty in Boys

THIS POST IS PART TWO OF TWO, ABOUT TODAY’S PAGE OF TALMUD.

On this page of Talmud we read of Rava's observation that delayed puberty may be related to body mass:

יבמות צז, א

כי אתו לקמיה דרבא אי כחוש אמר להו זילו אבריוהו ואי בריא אמר להו זילו אכחשוהו דהני סימנין זמנין דנתרי מחמת כחישותא וזמנין דנתרי מחמת בריותא

Whenever people came to Rava [with a case of a man who had not developed pubic hair]  he would tell them, if [the man was] thin, ‘Let him gain weight’; and if they were overweight he would say ‘Go lose weight’; for these signs [of sexual maturity] are sometimes delayed as a result of emaciation and sometimes  as a result of obesity.   (Yevamot 97a)

There has been some discussion of what appears to be the increasingly earlier onset of puberty in girls. In fact, menarche, (the age of a girl's first menstrual period) has been steadily decreasing by a consistent three years per century of record keeping. In an article in The New York Times published only a couple of weeks ago, the headline read “Puberty Starts Earlier Than It Used To. No One Knows Why.” It noted that “some girls are starting to develop breasts as early as age 6 or 7.”

However, Rava was addressing not the early onset of puberty in girls, but its delayed appearance in boys.  He noted that this delay was sometimes related to extremes of nutritional status, and so in these cases, was amenable to intervention.

“Rava may have been the first first to report an association of obesity and delayed puberty in boys.”

Rava was on to something. He may in fact have been the first to report an association between obesity and delayed puberty in boys.  This association has been confirmed by several studies which found that obesity has different effects on puberty in boys and girls. In girls, obesity is associated with earlier puberty, while in boys it has the opposite effect, and delays sexual maturation. But it was not until 2010 this association was confirmed by a longitudinal population-based study. This reported that a "higher BMI z score trajectory" (i.e. obesity)  during early to middle childhood may be associated with later onset of puberty among boys. 

Rava also claimed that puberty may be delayed in boys who are underweight, and this has also been confirmed. As far as I can tell, none of the researchers has credited Rava (who died around 350 CE.) for being the first to notice these associations. But Rava was first, and firsts count for something in science.

Rabbi Hiyya’s claim

The same passage is repeated in Bava Basra (155b) but in the name of Rabbi Hiyya.  Hiyya probably lived in the second half of the second century, and so predated Rava by a few decades.  The claim of primacy regarding the association with nutritional status and delayed puberty may therefore have to be extended back to R. Hiyya.  But so far I have found nothing in the works of Hippocrates, Aristotle and Galen that address this issue, so this association does not appear to have been a widely held belief in antiquity that was simply being echoed in the Talmud. As all good scientific papers end, further research is needed...

Niddah 48a - The Effect of the Environment on Puberty

Continuing an exploration of all things pubertal, the famous Rabban Shimon ben Gamliel suggests that the onset of puberty depends on where you live. Rabbi Shimon thinks that it depends on your social-economic background.

נדה מח,א

תניא רשב"ג אומר בנות כרכים תחתון ממהר לבא מפני שרגילות במרחצאות בנות כפרים עליון ממהר לבא מפני שטוחנות ברחים ר"ש בן אלעזר אומר בנות עשירים צד ימין ממהר לבא שנישוף באפקריסותן בנות עניים צד שמאל ממהר לבא מפני ששואבות כדי מים עליהן ואיבעית אימא מפני שנושאין אחיהן על גססיהן 

It is taught in a baraita, with regard to the appearance of signs indicating puberty in young women, that Rabban Shimon ben Gamliel says: In the case of young women who reside in cities, the lower sign [pubic hair] appears more quickly than the upper sign [breast growth], because they frequent the bathhouses, which stimulates the growth of the hair. By contrast, in the case of young women who reside in villages, the upper sign appears more quickly than the lower sign, because they grind with mills, which develops their breasts. 

Rabbi Shimon ben Elazar says: There are differences in the rate of development of the breasts. In the case of the daughters of the wealthy, the growth of the breast on the right side arrives more quickly than that of the left side, as it rubs against their upper body cloaks, which are worn by the wealthy. By contrast, in the case of the daughters of the poor, the growth of the breast on the left side arrives more quickly than that of the right side, because they draw jugs of water on that side. And if you wish, say instead that the left breast develops more quickly because they carry their younger brothers on their left sides.

Factors that influence Puberty

We have already learned that according to Rabbi Hiyya there is a relationship between body weight and the onset of puberty, a concept that has been firmly supported by modern research.  On today's page of Talmud Rabban Shimon ben Gamliel suggests that the environment can also influence the onset of puberty. And he was right. There is plenty of evidence from across the world that pubertal development differs between urban and suburban children.

In 1992 researchers compared the pubertal development of seventh graders in rural Iowa and suburban Chicago. They found that in general, the rural girls and boys were more developed than their suburban counterparts. A 2012 study published in the Annals of Human Biology found that there may be different demographic patterns in pubertal status among rural youth compared with urban youth in the US, but the researchers made it hard to figure out which group might be delayed.

Other studies comparing pubertal development among rural and urban youth, primarily from outside the US, consistently report a delayed onset of puberty in rural adolescents as compared to their urban counterparts. For example, a study published in 2000 examined "the prevalence of the first ejaculating emission" for 83,902 Chinese boys aged 9 through 18 years. It found a significant difference between urban and rural  boys and even plotted this out on a nice graph, shown below.

Prevalence of post- spermarcheal boys with ages in Chinese urban, rural, and their combined total group. From Cheng-Ye J. and Ohsawa S. Onset of the Release of Spermatozoa (Spermarche) in Chinese Male Youth. Am. J. Hum. Biol. 2000: 12;577–587.

They also found that within a single ethnic group there were significant geographic variations; the age of spermache was later for boys living in the north (where it is colder and wetter) compared to those living in the south (where it is hotter and more humid). However, in contrast to the 1992 US study, the urban Chinese boys had a later onset of puberty. Go figure.

Urban and Rural Children in Kazakhstan and beyond

Another study examined “Puberty in modernizing Kazakhstan”and compared rural and urban children. It used the Kazakhstan Health and Nutrition Examination Survey (KHAN-ES) that studied the effects of the living environment on the nutrition and health of urban and rural Kazakh children. In this study, the researchers reported the relationship between the environment, ethnicity and pubertal status in KHAN-ES children. They found that the environment had a strong influence on the timing of puberty. The rural children had a delayed puberty as compared with urban peers and this was especially evident at B2 and G2 stages

Something is going on. Perhaps rural adolescents have differential environmental exposures compared with urban or suburban adolescents, and some of these may change the rate of pubertal development. A study that examined the age of menarche (the first menstrual period) showed variability across many countries. In Israel, for example, the average age of menarche was 13.3 years; in Nepal it was 16.2 years. Here is what it looks like globally:

Variability of Ages at Menarche and Menopause. From here.

We still have a lot of work to figure out the complex interactions of all the factors that determine the onset of puberty. But both Rabban Shimon ben Gamliel and Rabbi Shimon ben Elazar were correct in linking the environment and socio-economic factors to the way in which our children develop into adults.