The Pubertal Transition And Menarche

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Menarche, the first menstrual bleeding, is understood by many to signal the onset of a woman's reproductive life. Yet, as will be described herein, the pubertal transition takes place over several years, with menarche occurring not at the onset, but relatively late in the process. Moreover, in most cases, women are not fertile (i.e., capable of becoming pregnant) until some period of time after menarche. This section will examine whether vegetarianism affects the pubertal transition, first by describing the transition itself, followed by an assessment of whether nutrition-related variables influence it. Finally, the available data comparing the age at menarche between vegetarians and omnivores will be evaluated.

A. The Pubertal Transition

In girls, the onset of puberty is marked by breast budding and the development of pubic and axillary hair. Both breast and pubic hair development progress through characteristic stages, described by Tanner as Stages 1 through 5, with Stage I representing prepubertal characteristics and Stage 5, full maturity.1 The age at which pubertal changes begin and their rate of progression vary considerably among individuals, although on average in North America, the pubertal transition begins at age 10-11 years (range 8-13).2 Initiation of breast development usually occurs first, and is followed by initiation of pubic hair development, peak height velocity, and menarche, respectively. Menarche usually occurs at a Tanner Stage of 3-4 for breast development. The first menstrual bleedings, however, are not usually associated with ovulatory cycles, and the establishment of regular ovulatory cycles does not occur for several years. For example, only 15% of cycles are ovulatory in the first year after menarche, 58% in the fourth year, and 74% in the sixth year.3

The outwardly visible external changes associated with puberty reflect the exposure of sensitive tissues to the gonadal hormones, particularly estrogen. Increased release of estrogen from the ovaries is stimulated by increases in the pulsatile release of the pituitary gonadotrophic hormones, luteinizing hormone (LH) and follicle-stimulating hormone (FSH). The increase in LH is particularly large, with mean daytime LH levels rising 60-fold between prepuberty and early puberty.3 In turn, the increased LH and FSH release result from the increased release of gonadotropin-releas-ing hormone (GnRH) from the hypothalamus.

The initiation of puberty does not appear to depend on the gonads' or pituitary's reaching a certain level of maturity, as both tissues are capable of responding to hormonal stimulation much earlier than normally occurs. For example, pulsatile administration of exogenous GnRH to very young female monkeys will initiate ovulatory menstrual cycles.4 Similarly, exogenous GnRH administration to young women with anorexia nervosa and delayed puberty will also induce the onset of pubertal changes and menarche.5 The causes of the increased activity of the GnRH pulse generator at the onset of puberty are not, however, known with cer-tainty.3

B. Factors Associated with Pubertal Onset and Menarche

There is abundant evidence that overall nutritional status, especially the balance between energy intake and expenditure (often reflected by height, weight, or body composition) is an important modulator of the onset of puberty.6-8 As reviewed by Bongaarts,7 several lines of evidence are available to support this relationship in humans. On average, puberty occurs earlier in well-nourished than in poorly nourished girls,9 and in those who have a higher weight-for-height at a given age. Since the end of the last century, mean age at menarche has decreased by about 3 years, and this has been associated with both improved diets and an increase in body size. Finally, age at menarche and socioeconomic status (SES) are negatively related in many countries, with differences observed between urban and rural populations and between high- and low-income groups.7

1. Body Size Variables

Although the data relating age at menarche to height and weight are convincing and relatively consistent at the population level, these variables are poor predictors at the individual level. A prospective study of 633 prepubertal girls, initially aged 8-10 years, obtained data on growth (height and weight measured at monthly intervals), exact age, height, and weight at menarche, health status, age at menarche of mother and sisters, adult height and weight of both parents, and SES.10 The girls, most of whom were Caucasian and middle-class, had heights and weights that were similar to U.S. norms. The most striking finding from this study was the extreme variability in the results. Mean age at menarche was 12.8 ± 1.2 years (range 9.1-17.7 years), mean height was 156.6 ± 6.4 cm (range

  1. 9-177.8 cm) and mean weight was 47.3 ± 6.9 kg (range 31.3-81.6 kg). There was also great variability in relative weight: mean Body Mass Index (BMI) was 19.3 ± 0.8 kg/m2, and ranged from about 13.5-29.7 kg/m2. Although a significant association between age at menarche and relative weight was observed (higher relative weights in those who were younger at menarche), the proportion of the variance accounted for by this association was just over 7%.10
  2. Diet Composition

As is evident from the above discussion, although associations exist between body size variables and age at menarche, much of the variability remains unexplained. Accordingly, it has been hypothesized that diet composition and, in particular, a high-protein, high-fat diet, may contribute to an earlier age at menarche.11 For example, rats reared on a high-fat diet grew more rapidly and reached estrus earlier and at a lower weight than those reared on a low-fat diet.12

The available human evidence for an effect of diet composition is not as direct as that provided by the animal data, and it is sometimes difficult to separate effects of diet composition from those of energy intake, which in turn is associated with body size variables. However, suggestive evidence is provided by a study of 233 Slovenian girls for whom the exact date of menarche was known.13 In this study, published in 1956, the mean age at menarche was 13.6 ± 1.2 years. The 45 girls who consumed a "proteinaceous" diet were significantly younger at menarche than the 75 who consumed a "mixed" diet (12.6 ± 0.9 vs. 13.4 ± 1.2 years), who in turn were significantly younger than the 110 girls who consumed primarily "carbohydratic" food (14.1 ± 1.6 years). Unfortunately, no data on actual nutrient intakes were obtained, and the girls classified their diets themselves. The authors attempted to address the effects of body size by observing the girls in gym class and classifying their body type as "baroque" (heavy), "renaissance" (medium) and "gothic" (thin). Direct measurements of height and weight, however, were not conducted. As expected, menarcheal age was youngest in the girls classified as heavy and oldest in those classified as thin. However, differences associated with diet persisted even when body type was considered. For example, among girls classified as heavy, menarche occurred at 12.4 ± 0.9 years and 13.9 ± 1.4 years for those consuming high-protein and high-carbohydrate diets, respectively. For girls classified as having medium body builds, the comparable ages were 12.9 ± 0.8 years and 13.8 ± 0.8 years.

Other data cited in support of this hypothesis are those of Burrell et al.,14 who studied approximate age at menarche in South African Bantu girls. Almost 50,000 girls aged 10-18 living in Transkei were asked whether menarche had occurred, and were assessed according to whether their home conditions were "poor" or "not poor." Mean age at menarche was 15.4 years for the "poor" girls, significantly older than the mean of 15.0 years for those who were "not poor." The authors suggest that differences in diet, in particular, animal protein, may have contributed to their observations. The "not poor" girls received a fermented milk drink daily and ate beef and poultry weekly, whereas "poor" girls consumed very little animal protein. Unfortunately, because height and weight for the two groups were not reported, it cannot be determined whether these dietary differences were also associated with differences in body size.

More recently, results have been reported from prospective cohort studies that included assessment of height and weight. A cohort of 2299 fifth-grade girls completed three 3-day diet records and was followed to determine when menarche occurred. No associations were found between intakes of any nutrient and age at menarche.15 Similarly, in a study of 213 premenarcheal girls whose diets were assessed using a semiquantitative food-frequency questionnaire, no associations between age at menarche and macronutrient intakes were observed.16 These studies did not assess the intakes of animal vs. plant proteins, but in the latter study, saturated fat intake was nonsignificantly associated with later age at menarche, suggesting that high intakes of animal products were not a determinant of early menarche.16

C. Studies of Age at Menarche of Vegetarians and Omnivores

As alluded to by the above discussion, although much remains to be learned about determinants of age at menarche, the overall plane of nutrition appears to be an important factor. Accordingly, when examining studies that compare age at menarche of vegetarians and omnivores, it is important to assess whether long-term energy balance is similar. The available data on the growth of vegetarian children are further examined in other chapters in this volume. Taken together, however, studies suggest that, given similar socioeconomic conditions, the heights and weights of vegetarian children do not differ substantially from those of omnivorous children. Thus, to the extent that growth variables modulate pubertal development, one would not anticipate differences between similarly nourished vegetarians and omnivores. If differences were observed, the inference would be that diet composition is a determinant of pubertal progression.

Few data are available that compare age at menarche between vegetarians and omnivores. Perksy et al. studied 35 vegetarian and 40 nonvegetarian teenage girls.17 The vegetarian girls were students at a Seventh-Day Adventist boarding school where a lacto-ovo-vegetarian diet was provided, and the non-vegetarians were students at a private boarding school in the same city. The diets of the two groups were similar in energy content, but the vegetarians' diets were significantly lower in total fat (33.7 vs. 39.7% of energy), saturated fat (12.3 vs. 15.5% of energy) and protein (13.0 vs. 15.1% of energy). Vegetarian girls also had higher intakes of starch and fiber, and lower intakes of sucrose and caffeine. Vegetarian girls were 2 inches shorter than non-vegetarians (P < 0.05), but the groups did not differ in weight, and means for BMI were very similar (22.8 ± 3.8 and 22.2 ± 4.2 kg/m2 for vegetarians and non-vegetarians, respectively), as were physical activity levels. More of the vegetarians were Hispanic (34.3% vs. 2.5%); whether this difference in ethnicity may have contributed to the observed height difference was not reported, but the possibility should be considered. Self-reported mean age at menarche was 12.4 ± 1.3 years in both the vegetarian and the omnivorous girls. Thus, in this group with different diets but apparently similar energy balance, differences in age at menarche were not observed.

Age at menarche was also compared between vegetarians and omnivores in an earlier cross-sectional study of acne conducted by Hardinge et al.,18 available only in abstract form, with additional details provided in an article by Sanchez et al.11 The 481 girls, all of whom were students at private schools, included 325 non-vegetarians and 156 vegetarians. Age at menarche was reported to the nearest 0.5 year, and was classified as early (<11.5 years), average (11.5-13.5 years) or late (>13.5 years). Among non-vegetarians, 20% had an early menarche and 21% had a late menarche. In contrast, only 13% of vegetarians had an early menarche, and 28% had a late menarche. The difference in distributions was significant (P < 0.05). Unfortunately, whether this difference reflects the influence of a vegetarian diet, or of differences in energy balance, cannot be ascertained, since data on heights and weights of these groups were not provided.

The above studies have compared age at menarche between American vegetarians and non-vegetarians. This issue has also been explored in southern India, in a study of 1267 girls aged 9-18 years from three schools differing in SES.19 All schools included both vegetarian and non-vegetarian subjects, and diets of all girls were primarily based on rice and wheat. Among vegetarians, these staples were supplemented with vegetable side dishes, whereas non-vegetarians also included mutton, fish, eggs, or fowl about 3-5 times per week. In this study, age at menarche was 12.86 years for girls at the school with the highest SES and 14.08 years for those at the poorest school. No effect of diet was observed, nor was there an interaction between diet and school. Conversely, another study from India reported that vegetarian girls had a significantly later age at menarche than non-vegetarians (13.7 ± 1.2 vs. 13.0 ± 1.2 years, P < 0.01).20 In that study, however, higher SES was also associated with earlier age at menarche, and it was not reported whether vegetarian and non-vegetarian girls had similar SES, nor were heights and weights reported. Accordingly, the results were potentially confounded by differences in SES or body size.

In summary, the available data suggest that, when food is freely available, age at menarche does not differ between vegetarians and non-vegetarians.

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