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Opposing Influences of Prenatal and Postnatal Growth on the Timing of Menarche

Institute of Diabetes and Endocrinology (C.S.T., S.P.G., C.T.C.), The Children’s Hospital at Westmead, Westmead, New South Wales 2145, Australia; Department of Pediatrics (F.d.Z.), University of Leuven, 3000 Leuven, Belgium; and Discipline of Paediatrics and Child Health (L.A.B., C.T.C.), The Children’s Hospital at Westmead Clinical School, University of Sydney, Westmead, New South Wales 2145, Australia

Address all correspondence and requests for reprints to: Charmaine Tam, Institute of Diabetes and Endocrinology, The Children’s Hospital at Westmead, Westmead, New South Wales 2145, Australia. E-mail: charmait{at}chw.edu.au.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Context and Objective: Menarche is a milestone of reproductive development, and its timing may be differentially influenced by the growth conditions before birth and those between birth and puberty. The present study explored the relationships among menarcheal timing and markers of prenatal and midchildhood growth in healthy Australian girls.

Setting, Design, and Patients: A total of 156 girls aged 8 yr from a birth cohort of full-term babies had height, weight, and waist circumference measured. One hundred three girls had dual x-ray absorptiometry performed and blood analyzed for insulin, leptin, IGF-I, estradiol, and dehydroepiandrosterone sulfate levels. Girls were followed up at age 15 yr and their age of menarche was recorded.

Main Outcome Measures: Measures included age of menarche; birth weight and birth length; height, weight, waist circumference, and body composition by dual x-ray absorptiometry; and plasma insulin, leptin, IGF-I, estradiol, and dehydroepiandrosterone sulfate at age 8 yr.

Results: Girls with earlier menarche were light and long at birth and had higher total and central adiposity and IGF-I and estradiol levels in midchildhood, compared with those with later menarche. Age of menarche was best predicted by combining size at birth and body mass index z score at age 8 yr (r² = 0.12; P < 0.001).

Conclusions: The timing of menarche appears to be influenced in opposing directions by pre- and postnatal growth. Menarche was found to occur earlier in girls who were long and light at birth and who had a higher fat mass and circulating IGF-I in childhood. These findings may partly explain ethnic differences and secular trends in the age of menarche.

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OVER THE PAST century, the average menarcheal age has advanced considerably (1, 2), and this may become cause for concern because an earlier timing of menarche has been associated with a higher risk for adult diseases such as metabolic syndrome and breast cancer (3, 4, 5). The timing of menarche is known to be determined by factors including body mass index (BMI), socioeconomic status, physical activity, nutritional status, and genetic influences, the latter explaining half of the variance in menarcheal timing (2, 6, 7, 8, 9, 10).

Recent studies examined whether the intrauterine environment may also influence menarcheal timing; the results have been inconsistent, possibly in part because of the heterogeneity in the study designs (11, 12, 13, 14, 15, 16, 17). English and Swedish girls, who were lighter at birth, were found to attain menarche on average 2–5 months earlier than girls who were heavier at birth (12, 18). In Catalan girls with early-normal onset of puberty, menarche was also found to occur earlier among those with a low birth weight (14).

Here we present the first longitudinal study that explored the relationships among size at term birth; body composition [assessed by anthropometry and dual-energy x-ray absorptiometry (DXA)] and hormone levels [circulating insulin, leptin, IGF-I, estradiol, and dehydroepiandrosterone sulfate (DHEAS)] in midchildhood; and age of menarche in healthy Australian girls.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The girls in this study were originally recruited for a broader study designed to investigate the effect of birth size, body size, and genes on blood pressure and bone density. All were born at term (mean gestational age 40 wk, range 37–42 wk) at Nepean Hospital, Penrith, in western Sydney between August 1989 and April 1990 and were part of a birth cohort (n = 2314) whose details and selection criteria have been previously published (19, 20). The children were predominantly (>96%) of European descent. Written consent was obtained from participants and their parents. The Children’s Hospital at Westmead Ethics Committee and The Ethics Committee of the Wentworth Area Health Service approved the study.

In 1996–1997, 215 girls (aged 8 yr) were recruited, and their anthropometry was measured. A subset of this cohort (137 girls) had a fasting blood sample obtained. One hundred fifty-six girls were followed up in 2004 (aged 15 yr), of which a subset of 103 had blood taken and body composition measured using DXA at age 8 yr. A total of 149 girls had complete birth, anthropometry, and menarche data. Seven girls had not commenced menarche by age 14.8 yr [mean age (n = 7) 14.9 yr, range 14.8–15.2]. For categorical analysis, these girls were included in the late menarche group.

At age 8 yr, there were no significant differences between girls who participated in this study (n = 156) and girls who did not participate (n = 59) in terms of height, weight, and BMI (raw values and z scores). Nonparticipants were 160 g heavier (P = 0.003) and 10 mm longer (P < 0.001) at birth. The participation rate in this study was 63%, which is similar to previous cohort studies (21).

One girl’s data had an undue influence on statistics; her data are not included in the tables or figures but are discussed separately in the Results. She was a relatively long and heavy baby (3.6 kg, 51.0 cm) and had late menarche (13.8 yr). At age 8 yr, her BMI was 21.35 kg/m² (BMI z score 1.75), circulating IGF-I levels 19.7 nmol/liter, leptin 7.9 ng/ml, and DHEAS 1.8 µmol/liter. She had 15.0 kg fat, 43.7% body fat, and 0.92 kg abdominal fat; all these values were more than 3 SD away from the mean of the total cohort and at least 4 SD away from the mean of the late menarche group.

Anthropometry at birth

Gestational age, birth length, birth weight, and head circumference were obtained from the hospital medical records, and ponderal index [weight (grams)/birth length (cubic centimeters)] was calculated.

Anthropometry at 8 yr

At 8 yr of age, height, weight, and waist circumference were measured using standard techniques by research assistants trained by an accredited anthropometrist (22). Waist circumference was measured to the nearest 0.1 cm with a flexible steel tape at the level of the narrowest point between the lower costal border and the iliac crest. If there was no obvious narrowing, the measurement was taken at the midpoint between the two landmarks. BMI (weight/height squared; kilograms per square meter), height, weight, waist circumference (23), and BMI age- and gender-specific z scores were calculated (24). The International Obesity Task Force BMI cut-points were used to define overweight and obesity (25). Puberty was not formally assessed, but the children were viewed in undergarments during anthropometric assessment, and none were overtly pubertal.

DXA

Total body fat, fat-free soft tissue, leg fat, abdominal fat, and trunk fat tissue were measured using DXA (Lunar DPX equipped with proprietary Lunar DPX software, version 3.6; Lunar Corp., Madison, WI). The experimental procedure has been described previously (20, 26, 27). Briefly, the fast scan mode and standard subject positioning were used for total body measurements and were analyzed using the extended analysis option. Manual analysis, using the regions of interest feature, was performed on total body scans to gain specific information about the abdominal region, which was defined by anatomic bony landmarks. The upper border was defined as the distal margin of the lower ribs and the lower border, just superior to the suprailiac crest. The lateral margins were placed outside the body so that all abdominal but no arm tissue was included. Similar to studies by Hogler et al. (28) and Sachdev et al. (29), fat-free soft tissue was adjusted for height.

Biochemistry

Morning blood samples were collected by venepuncture after an overnight fast. Plasma was frozen at –20 C until assayed. Assays (insulin, IGF-I, leptin, DHEAS, and estradiol) were conducted by the Endocrine Laboratory at the Children’s Hospital at Westmead (26, 27). Briefly, DHEAS levels were determined with the use of an in-house competitive binding RIA. Commercial RIAs were used to determine concentrations of insulin (Linco Research, Inc., St. Charles, MO), IGF-I (Bioclone Australia Pty. Ltd., Sydney, Australia), leptin (Linco Research), and estradiol (DiaSorin, Saluggia, Italy).

Age of menarche

At age 15 yr, girls were asked via questionnaire whether they had attained menarche and the month and year of their first menstrual period. For analysis, girls were categorized into three groups: early (<11.5 yr), average (11.5–13.7 yr), and late (>13.7 yr) menarche. The age limits of these groups were defined by mean age of menarche ± 1 SD (11).

Data analysis

The primary outcome measure was age of menarche. ANOVA and independent sample t tests were used to compare normally distributed data, and the Kruskal Wallis and Mann Whitney U tests were used for data, which were not normally distributed. Pearson’s correlation and Spearman’s rho tests were used to assess correlations among birth size, anthropometry and hormone levels at age 8 yr, and age of menarche. The comparison of menarche in the birth size groups was conducted using analysis of covariance with BMI z score at age 8 yr as a covariate.

Multiple regression models were developed to examine whether menarcheal age was related to birth size (weight, length, and birth size group); anthropometry at 8 yr (weight, height, waist circumference, BMI); and hormone levels at 8 yr (insulin, IGF-I, leptin, DHEAS, estradiol). Dummy variables were used for analyzing birth size group. Indicators for collinearity were examined, and residuals of the final model were normally distributed.

Data were analyzed using Statistical Package for Social Sciences, version 11.5. (SPSS, Chicago, IL). Data are presented as mean ± SD or median (range).

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The mean birth weight was 3.36 ± 0.50 kg. Five babies were less than 2.5 kg. The mean age of menarche was 12.6 yr (range 8.9–14.8 yr), with 95% of girls attaining menarche by age 14.8 yr (n = 149 of 156). Birth details, anthropometry, and hormone levels are presented in Tables 1 and 2.

Girls with late menarche (>13.7 yr; upper tertile) had significantly lower weight, BMI, and waist circumference, total body fat, percent body fat, percent abdominal fat and percent trunk fat at 8 yr compared with girls with early (<11.5 yr; lower tertile) and average (11.5–13.7 yr; middle tertile) menarche. Girls with early menarche had at age 8 yr significantly higher estradiol and IGF-I levels, compared with girls with average and late menarche.

When the outlier was included in the analysis, there was no difference in total body fat (P = 0.130), percent body fat (P = 0.124), trunk fat percent (P = 0.084), and abdominal fat (P = 0.083) among the menarche groups.

Age of menarche and birth size

There were no correlations between age of menarche and birth size (weight and length). Girls were classified into four birth size groups: long light (n = 15), long heavy (n = 59), short light (n = 59), and short heavy (n = 15), defined using median values for birth weight (3325 g) and length (49.3 cm), as reported by Adair (11). After adjusting for BMI z score at 8 yr, girls who were classified as long light at birth attained menarche 1 yr earlier (age of menarche ± SEM: 12.0 ± 0.3 yr) than girls who were short heavy (13.0 ± 0.3 yr) and about 6 months earlier than girls who were long heavy (12.5 ± 0.1 yr) or short light (12.6 ± 0.1 yr). Similar results were found when adjusted for percent body fat.

Age of menarche, anthropometry, and hormones

Age of menarche was inversely associated with BMI (r² = 0.08, P < 0.001), weight (r² = 0.06, P < 0.001), waist circumference (r² = 0.06, P < 0.001) (raw values and z scores), percent body fat (r² = 0.07, P = 0.027), and circulating IGF-I (r² = 0.05, P = 0.030) and leptin (r² = 0.05, P = 0.024) levels at age 8 yr.

Birth weight, body composition, and hormones

Birth weight was positively associated with weight (r² = 0.06, P = 0.001), height (r² = 0.10, P < 0.001), waist circumference (r² = 0.03, P = 0.038) (raw values and z scores), total body fat (r² = 0.07, P = 0.026), fat-free soft tissue (r² = 0.16, P < 0.001), and fat-free soft tissue adjusted for height (r² = 0.11, P = 0.001) at 8 yr but not with BMI or percent body fat. There was a negative association between birth weight and estradiol (r² = –0.11, P = 0.001) and a positive association between birth weight and insulin (r² = 0.04, P = 0.035).

Multiple regression analysis

The influence of adiposity (weight, BMI, waist circumference, total body fat, trunk fat, and abdominal fat), hormones (insulin, IGF-I. leptin, DHEAS, and estradiol) in midchildhood on age of menarche was examined. The strongest predictors of age of menarche were BMI z score at 8 yr, which predicted 9% of the variation in age of menarche. When birth size group was included in the model, the variation explained increased to 12%. As shown in Fig. 1A, girls who were born long light and had a BMI z score greater than 0 at 8 yr had earlier menarche, compared with girls who were born short heavy and had a BMI z score 0 or less. This difference was readily apparent around age 13 yr; 71% of the girls who were born short heavy and had a lower BMI at age 8 yr were still premenarcheal, whereas all the girls who were born long light and had a higher BMI at 8 yr were already postmenarchal (Fig. 1B).

View larger version (25K): [in this window] [in a new window]   FIG. 1. Birth size and BMI z score at 8 yr predict age of menarche. A, Girls who are long light at birth and heavier at age 8 yr attain menarche earlier on average. B, The percentage of premenarchal girls at age 13 yr is displayed by birth size and BMI z score groups. At age 13 yr, all girls who were long and light at birth and had high BMI z score at 8 yr had attained menarche. The outlier was not included in the figure.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Menarche is traditionally regarded as the beginning of reproductive life. Alternatively, menarche could be viewed as the end of a delicately balanced process that spans both pre- and postnatal life up into late puberty. Here menarcheal age was found to be linked to birth size, body size, and composition and the endocrine status in midchildhood. The girls with the earliest menarche were long light at birth, were centrally more adipose, and had higher circulating IGF-I levels in midchildhood. In contrast, the girls with the latest menarche were shorter and heavier at birth and were leaner with lower IGF-I levels at age 8 yr. These findings indicate that the timing of menarche is, just like adrenarche (30), influenced in opposing directions by pre- and postnatal growth, as judged by the above-mentioned markers that, in turn, may be interrelated. The recognition that pre- and postnatal growth exert opposing effects on menarcheal timing allows to reconcile many apparent inconsistencies in the previous literature on this topic (11, 12, 13, 14, 15, 16, 17).

Mathematically, prenatal weight-vs.-length gain and postnatal weight for height may have opposing influences on the timing of menarche; physiologically, however, they could be parallel phenomena. Indeed, prenatally reduced weight gain results in a loss of fat-free soft tissue rather than in a loss of fat mass (31). After catch-up weight gain in infancy, children with a low birth weight-for-gestational-age tend to develop a relatively high fat fraction, even when not obese; in other words, a low weight for length at birth tends to be followed by a high ratio of fat over lean mass and relative insulin resistance in early childhood (32). A high weight for height (or BMI z-score) in midchildhood is, after adjustment for prenatal growth, also associated with a higher fraction of total and central fat and relative insulin resistance (20, 33). The apparently opposing influences of pre- and postnatal gain in weight for height may thus reflect forces that point physiologically in the same direction, namely toward body adiposity and insulin resistance. In turn, circulating IGF-I may be a reflection of the latter, because insulin-sensitizing metformin therapy is known to lower IGF-I levels in girls with low birth weight and delay their pubertal development up to menarche (34, 35). Collectively, the present findings corroborate the concept that body adiposity, possibly in part through hyperleptinemia, and insulin resistance are key contributors to the normal variation in the timing of menarche. It is possible that much of the so-called ethnic and secular variation (2, 3) in the timing of menarche will prove to be attributable to the determinants disclosed here, including prenatal gain of weight vs. length and postnatal weight for height, body adiposity, and their correlates such as insulin resistance and circulating leptin and IGF-I.

The present findings may have implications for the development of non-GnRH agonist-mediated approaches to delay the feminine development of girls at risk of early menarche. In nonobese girls born long light, fat mass and circulating IGF-I and leptin can be reduced by giving an insulin sensitizer like metformin, and there is already evidence indicating that such treatment indeed delays menarche toward a more average age (34, 35).

A negative relationship among age at menarche, BMI, and body fatness in girls has been reported in some studies (36, 37). However, it is still unclear whether increased childhood adiposity causes earlier menarche, earlier menarche induces an increase in body fat later in life, or both of these phenomena cooccur (38). We were unable to evaluate this interaction in our study. Associations do not allow inference of causality; our finding of increased body weight at age 8 yr may not cause early menarche but could be an indicator of early puberty and reflect the immediate prepubertal gain in weight seen in normal children.

Potential limitations of this study are that we were unable to account for the influence of genetics on the age of menarche. The influence of genetics is estimated to be half of the variance in menarchal timing (7), with previous studies using maternal height and age of menarche to account for this influence (11, 16). However, Romundstad et al. (16) reported that adjustment for these maternal factors resulted in only a very moderate attenuating effect on the associations between birth size and age of menarche. A further limitation of this study is the small numbers in the birth size groups. Further studies in larger cohorts could be important in validating these findings.

At age 7–8 yr, puberty (breast budding) was not formally assessed. Although of interest, this limitation of the study is unlikely to have influenced the results significantly because mean age at menarche was 12.6 yr in the total study population, thus suggesting that mean age at B2 was likely between 10 and 11 yr (2) and that, at age 7–8 yr, less than 5% (or even < 3%) of the study girls were clinically pubertal.

In conclusion, the timing of menarche appears to be influenced in opposing directions by pre- and postnatal growth. Menarche was found to occur earlier in girls who were long light at birth and who had a higher fat mass and circulating IGF-I in childhood. These findings may partly explain ethnic differences and secular trends in the age of menarche.

	Acknowledgments

 
We thank all the families that generously donated their time to participate in this study.

	Footnotes

 
This work was supported by National Health and Medical Council Project Grant 20655501 and The Children’s Hospital at Westmead Grant Research Scheme. F.d.Z. is a clinical investigator of the Fund for Scientific Research, Flanders, Belgium.

The authors have nothing to disclose.

First Published Online August 22, 2006

Abbreviations: BMI, Body mass index; DHEAS, dehydroepiandrosterone sulfate; DXA, dual-energy x-ray absorptiometry.

Received May 4, 2006.

Accepted August 10, 2006.

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