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The Journal of Clinical Endocrinology & Metabolism Vol. 90, No. 5 2718-2724
Copyright © 2005 by The Endocrine Society

Early Menarche and the Development of Cardiovascular Disease Risk Factors in Adolescent Girls: The Fels Longitudinal Study

Karen E. Remsberg, Ellen W. Demerath, Christine M. Schubert, Wm. Cameron Chumlea, Shumei S. Sun and Roger M. Siervogel

Lifespan Health Research Center, Department of Community Health, Wright State University School of Medicine, Kettering, Ohio 45420

Address all correspondence and requests for reprints to: Dr. Karen E. Remsberg, Lifespan Health Research Center, Wright State University School of Medicine, 3171 Research Boulevard, Kettering, Ohio 45420-4006. E-mail: karen.remsberg{at}wright.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
The purpose of this study was to evaluate the influence of menarcheal age on changes in insulin, glucose, lipids, and blood pressure during adolescence and to assess whether body composition modifies this relationship. We examined 391 girls, a subset of Fels Longitudinal Study female participants (8–21 yr of age). Self-reported menarcheal age was classified based on the National Health and Nutrition Examination Survey III distribution, in which early menarche was at the 25th percentile or less (11.9 yr). Age at menarche was examined in relation to measures of body composition [e.g. fat-free mass (FFM) and percent body fat (PBF)], insulin resistance, blood pressure, and lipid profile. The effects of menarcheal age and body composition on cardiovascular disease risk factor changes were analyzed with serial data mixed models. Median menarcheal age was 12.7 yr (range, 9.8–17.0 yr), with 91 girls (23%) classified as early menarche. Girls with early menarche had more deleterious changes in insulin, glucose, blood pressure, FFM, and PBF levels than girls with average or late menarche. Menarcheal age adversely affected cardiovascular disease risk factor changes independent of age and changes in FFM or PBF. Girls with early menarche exhibited elevated blood pressure and glucose intolerance compared with later maturing girls, independent of body composition.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
EARLY MENARCHE (EM) is associated with several reproductive and cardiovascular disease-related outcomes (1, 2, 3, 4, 5). In this context, early age at menarche is defined as the lowest quartile of menarcheal age based on the National Health and Nutrition Examination Survey III (6), instead of the clinical definition of greater than 2 SD below the national average. EM is also associated with both proximal and longer-term hyperinsulinemia and insulin resistance (7, 8), but reduced insulin sensitivity is a normal feature of the early stages of sexual maturation (9, 10). The pubertal transition has equivocal effects on lipid and lipoprotein levels (11, 12), but with the onset of sexual maturation, both systolic and diastolic blood pressures increase (13, 14). Early age at menarche is associated with a greater body mass index (BMI) and body fatness than are average and later age at menarche (15, 16), and elevated adiposity in adolescence is predictive of elevated adiposity in adulthood (17, 18). However, many studies of these cardiovascular disease (CVD) risk factors (i.e. adverse lipid and lipoprotein levels, elevated blood pressure, insulin resistance, and body fatness) did not use serial data to evaluate the longer-term effects of menarcheal timing.

Assessing the health of girls with early menarche will help to clarify the association between the timing of sexual maturation and CVD risk factors. Evaluation of longitudinal changes in CVD risk factors has shown that CVD precursors can be detected as early as late childhood. These CVD precursors along with body composition, lipids, blood pressure, and insulin resistance are internally consistent, (i.e. track) within individuals over time (19, 20, 21). Furthermore, body composition during adolescence is significantly associated with adult levels of fasting insulin, insulin utilization, blood pressure, and high density lipoprotein cholesterol (HDL), low density lipoprotein cholesterol (LDL), and total cholesterol (TC) (22, 23, 24).

Due to the inferred connections among future CVD risk, insulin resistance, increased adiposity, and early sexual maturity, our objective was to assess 1) the association of EM with an adverse adolescent CVD risk factor profile represented by insulin resistance and elevated blood pressure and lipid and lipoprotein levels, and whether 2) EM affects changes in CVD risk factors independent of the elevated body fat and lean mass found in early-maturing girls. Increased knowledge of these relationships will help in the clinical management of girls with EM in light of the pediatric obesity epidemic.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Sample

We examined the serial data collected from the visits of 391 white girls who participated in the Fels Longitudinal Study between 8–21 yr of age. A description of the Fels Longitudinal Study, a cohort of generally healthy individuals, has been published previously (25). Detailed health history questionnaires, body composition measures, fasting blood samples, and measures of CVD risk factors were obtained at annual examinations. All protocols and procedures regarding the observation and evaluation of study participants were approved by the Wright State University institutional review board. Study participants were apprised of planned study procedures, and they or their guardians signed informed consent statements in acceptance of the participant testing guidelines.

Data collection

Variables. Age at menarche was determined from the self-reported date of first menses based on biannually administered questionnaires. EM, average menarche (AM) and late menarche (LM) were classified according to published national estimates of the timing of menarche for non-Hispanic white U.S. girls derived from the National Health and Nutrition Examination Survey III (1988–1994) (6). These estimates were defined as less than or equal to the 25th percentile (≤11.9 yr) for EM, between the 25th and 75th percentiles (>11.9 to ≤ 13.2) for AM, and greater than the 75th percentile (>13.2 yr) for LM.

Anthropometry. Measurements of weight and abdominal circumference (AC) followed standardized procedures (26). Height was measured to 0.1 cm on a Holtain stadiometer (Seritex, Carlstadt, NJ), and weight was measured to 0.1 kg on an electronic scale. Central adiposity was estimated via AC, where a metric tape measure was used to measure circumference at the level of the anterior-superior iliac crest (27).

Body composition. Hydrodensitometry corrected for residual volume was used to determine body density to calculate total body fat mass (TBF), fat-free mass (FFM), and percentage of body fat (PBF) for each individual (17, 28). TBF, FFM, and PBF were computed from the body density estimate using age- and sex-adjusted equations based upon a multicomponent model (17).

Blood pressure. Systolic (SBP) and diastolic (DBP) blood pressures were measured in the right arm with the participant seated, following standard procedures (29).

Serum biochemical assays. Fasting blood samples were collected. Serum concentrations of insulin (microunits per milliliter) and glucose (milligrams per deciliter) and plasma concentrations of triglycerides (TG; milligrams per deciliter), TC (milligrams per deciliter), HDL (milligrams per deciliter), and LDL (milligrams per deciliter) were determined using standard assays. These assays were conducted at the Population Genetics Phenotyping Laboratory, Southwest Foundation for Biomedical Research (San Antonio, TX), and by the Medical Research Laboratory (Cincinnati, OH). The glucose-insulin ratio (GIR) was calculated by dividing fasting blood glucose by fasting insulin concentrations.

Statistical analysis

There were 4436 study visits for these 391 girls, with an average of 11 study visits/individual. Subsets of these data were analyzed for CVD risk factors; 391 girls had 4436 serial blood pressure observations, 210 girls had 1204 serial observations for body composition (PBF and FFM), 197 girls had 911 serial observations for lipids and lipoproteins, and 113 girls had 541 serial observations for insulin resistance. Girls were evaluated through annual examinations. Differences in numbers of observations for CVD risk factors stem from introducing the assessment of glucose and insulin into the Fels Study protocol at a later date than the procedures for blood pressure, body composition, and lipid measurement.

Descriptive statistics. The distribution of age at menarche in the sample population was examined and compared with national estimates of the 25th and 75th percentiles for white, non-Hispanic females. No race-stratified analyses were conducted. Each of the intended dependent variables [insulin, glucose, lipids, blood pressure, and selected measures of body composition (FFM, PBF, TBF, and AC)] was assessed for normality. Only insulin was log-transformed for analysis due to a skewed distribution. Cross-sectional means based on one observation per participant per age group were plotted and compared by single-year age and menarcheal groups for each variable. Statistical significance testing for differences in means between the menarcheal groups was assessed by ANOVA models.

Mixed effect model serial analysis. Using these serial data, mixed effect models were constructed, with age at menarche and chronological age as the independent continuous variables, and CVD risk factors as the dependent continuous variables. Age at menarche was treated as a fixed effect, whereas chronological age and the intercept were designated as random effects. These models were assessed with the statistical significance level for the variable estimates set at P < 0.05. Body composition variables were added to the mixed effects model to study the effect of age at menarche on CVD risk factor changes, adjusting for the independent effects of changes in body composition. These covariate body composition effects were treated as fixed. All statistical analyses were performed using the SAS version 8 statistical software package (SAS Institute, Cary, NC) (30).


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Descriptive statistics

The chronological age of these 391 girls at the time of their visits ranged from 7.27–20.99 yr. The median age at menarche was 12.73 yr (range, 9.80–17.00 yr). Based on national quartile estimates of the onset of menarche for non-Hispanic, white girls (6), the Fels Longitudinal Study sample of girls had the following distribution of menarcheal age; roughly 23% (n = 91) of the girls in this sample were classified as EM, 42% (n = 165) as AM, and 35% (n = 135) as LM. The age at menarche distribution and number of serial observations for subjects in each menarche group are shown in Table 1Go. Girls reporting EM had an average of 13 serial visits, whereas AM and LM girls had an average of 16 and 17 serial visits, respectively. The proportion of girls classified as EM (23%) was comparable to the national estimates for the first quartile, whereas the proportions of AM girls vs. the middle two quartiles and of LM girls vs. the uppermost quartile (42% and 35%, respectively) suggested later maturation than the national estimates.


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  		TABLE 1. Menarcheal age distribution and number of serial observations per subject

 
Means plotted by age for CVD risk factors and selected measures of body composition (insulin, SBP, FFM, and AC) are presented by menarcheal age groups (Fig. 1Go). The girls in the EM group tended to have higher SBP, FFM, and AC than the girls in either the AM or LM groups. SBP was significantly different between menarcheal groups for ages 8–14 and 16 yr, FFM was significant at ages 9 and 11–14 yr, and AC differed significantly for all age groups (8–18 yr of age). With the onset of puberty, EM girls had the highest insulin levels compared with the other groups, which were significant at ages 10–12 yr, but this relationship was not sustained throughout adolescence. There was an inverse relationship between age at menarche and insulin, SBP, FFM, and AC, where an earlier menarche indicated higher levels of each risk factor. No statistically significant differences were found among the age at menarche groups for DBP, TC, LDL, HDL, or glucose.



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  		FIG. 1. Cross-sectional means of CVD risk factors by menarcheal age group and age. Insulin data are given as microinternational units per milliliter (picomoles per liter). To convert from microinternational units per milliliter to picomoles per liter, multiply the microinternational units per milliliter amount by 6.945. Top row, FFM and AC; bottom row, SBP and insulin.

 
Serial analysis

Adjusting for chronological age, age at menarche was significantly associated with changes in insulin, glucose, GIR, SBP, DBP, AC, FFM, PBF, and TBF (Table 2Go). EM was associated with decreased GIR and increased insulin, glucose, SBP, and DBP levels. Throughout adolescence, blood pressure and body mass increased (and LDL decreased) with rising chronological age. Increasing chronological age did not create statistically significant positive changes in insulin, glucose, TC, or TG or negative changes in HDL or GIR levels. Menarcheal age was an important factor in explaining the variation in serial measures of body composition, AC, FFM, PBF, and TBF, where early menarche was related to higher mean levels and elevations in these body composition measurements. Chronological age accounted for only part of the significant inverse relationship between EM and positive changes in both lean and fat mass.


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  		TABLE 2. Mixed effects linear regression best model estimates (SE) of age at menarche, effects on CVD risk factors, and body composition variables, adjusted for age

 
An additional set of mixed effect models was constructed to test whether the elevation of CVD risk factors in early maturing girls is explained by differences in body composition (represented by FFM and PBF in separate models). Table 3Go shows the age- and body composition-adjusted parameter estimates for insulin, glucose, GIR, and blood pressure. There were statistically significant associations of early age at menarche with increased FFM and SBP, but not with insulin, glucose, GIR, or DBP. Among the models that included PBF, age at menarche independently influenced changes in GIR, insulin, SBP, and DBP. All models except for the two GIR models showed that earlier menarcheal age was associated with a higher level of the dependent CVD risk factor. EM was associated with a lower GIR, representing increased insulin resistance (higher insulin relative to glucose concentrations).


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  		TABLE 3. Best model parameter estimates (SE) for effect of age at menarche adjusted for age and either FFM or PBF for changes in glucose, insulin, and blood pressure

 
The effects of menarcheal age on lipids, lipoproteins, and AC, adjusting for age and FFM or PBF, are presented in Table 4Go. When age and either PBF or FFM were included as potentially mitigating factors, early menarcheal age remained a significant, independent correlate of increases in AC. However, there was no statistically significant effect of age at menarche on TC, TG, HDL, or LDL after age and body composition adjustment.


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  		TABLE 4. Best model parameter estimates (SE) for effect of age at menarche adjusted for age and either FFM or PBF for changes in lipids, lipoproteins, and AC

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
This study examined the associations among the timing of age at menarche, its relationship with CVD risk factors and their changes, and the possible intermediary effects of body composition on this relationship. Along with a greater increase in adiposity during adolescence, girls with EM have less favorable CVD risk factor changes compared with average or later maturing girls. Early menarcheal age was related to changes in a number of these specific risk factors, independent of changes in body composition and chronological age. Early maturing girls in the Fels Longitudinal Study were heavier and had more adiposity than average or late maturing girls across adolescence, as was seen in their higher values for AC, PBF, TBF, and FFM. These findings are supported by previous investigations in the Fels Longitudinal Study and in other study samples (31, 32, 33, 34, 35, 36, 37, 38).

After adjusting for the combined effects of age at menarche, chronological age, and FFM or PBF on CVD risk factors, age at menarche remained an independent predictor of changes in insulin, GIR, AC, SBP, and DBP. The effect of early menarche on CVD risk factors is only partially explained by the lean and adipose tissue components of body mass. Investigators from the Bogalusa Heart Study reported that the effect of menarcheal timing on adulthood obesity was ascribed largely to the intermediary effect of childhood obesity, ascertained through BMI and skinfold measurements, and minimally to EM (39). However, BMI does not accurately represent body composition in adolescence; lean and adipose tissue masses are accumulated differentially throughout this period (40, 41, 42, 43). The second aim of this study was to examine the potential modulating effects of body composition on CVD risk factors. In our results, menarcheal timing was associated independently with changes in both lean and adipose tissue components. In particular, earlier menarche was associated with increases in both adipose and lean tissue. Separately evaluating the effects of lean and adipose tissues refines the question of how body composition components and menarcheal age influence each risk factor.

The present examination of menarcheal age and CVD risk factors demonstrated that girls with EM had higher fasting insulin concentrations, comparable fasting glucose concentrations, and correspondingly low GIR compared with girls with average and late menarche. This effect remained after considering the influences of chronological age and PBF. Adjusting for FFM reduced the influence of EM on higher insulin and lower GIR levels, both modulated during adolescence more by skeletal muscle tissue than by central adiposity. Although insulin resistance is a recognized feature of the onset of the pubertal transition (9, 10), our study demonstrated that girls with EM tended to retain hyperinsulinemia and/or insulin resistance throughout puberty. To our knowledge, other studies of pubertal insulin resistance have not followed girls across adolescence to examine the longitudinal effects of menarcheal timing on patterns of insulin resistance.

In this study, early age at menarche was associated with increased SBP, even after adjustment for body composition. A similar, significant inverse relationship between age at menarche and DBP was found upon adjustment for either FFM or PBF. Blood pressure generally increases with the onset of puberty in girls (14, 44). Menarcheal age is correlated with blood pressure levels in both cross-sectional and longitudinal studies (13, 14), and blood pressure has been shown to track within individuals over time (21). The association of EM with increased blood pressure may be partially related to the fact that earlier maturing girls are taller at age 12 yr than average and late maturing girls (45, 46). During later adolescence, however, the relationship between height and maturation switches, and early maturing girls are shorter than average and late maturing girls.

The impact of age at menarche on lipoprotein and lipid concentrations is less clear. We reported that age at menarche had a mild inverse effect on changes in TG levels and did not significantly affect changes in lipoprotein levels. Previous cross-sectional and longitudinal investigations of lipoprotein and lipid concentrations in community-based populations have corroborated these results (11, 47). In Fels Longitudinal Study girls, concentrations of TC and LDL increase up to age 12 yr and then decline, and the concentrations of TG increase up to age 14 yr and then decline, whereas the concentrations of HDL remain virtually unchanged from age 8–18 yr (12). In the Princeton Maturation Study, TC fell in midpuberty with a reduction in HDL, and a late rise in TC levels was accompanied by rising LDL levels (11). In a cross-sectional comparison in the Bogalusa Heart Study, the correlations between sexual maturation and lipid and lipoprotein concentrations were very low or negative for TC, TG, and LDL and positive for HDL (47). Unlike the associations among EM, glucose metabolism, and blood pressure, at this point there is no clear evidence that EM consistently affects changes in lipid and lipoprotein levels during adolescence.

The primary strengths of this study were the availability of multiple measurements of CVD risk factors for girls throughout late childhood, adolescence, and into early adulthood and the ability to examine the impact of fat and FFM on these changes. It is possible to evaluate the influence of menarcheal age on the changes in CVD risk factors over time. The tracking of CVD risk factors among individuals from childhood to adulthood indicates that the propensity for disease can be evaluated during early life. Menarcheal age in the Fels Longitudinal Study population is reported within 6–24 months of onset, with 80% of the sample reporting within 6 months. Self-reported age at menarche has been shown to be a reliable assessment of menarcheal onset, i.e. up to 83% reliability with recall at 5 yr after menarche (48, 49). An average recall at 6 months is likely to have better reliability than the 5 yr postmenarche estimate.

Limitations of this study concern the sample characteristics, such as the sample size and that all of the girls were white, reducing the generalizability of the results. The moderate sample size did not allow for the inclusion of physical activity or sex steroid hormone concentrations as potential confounders in each predictive model. It was not possible to test the effects of ethnicity on menarcheal timing, where black girls reach menarche earlier than white girls (38). Adjusting statistically for body composition may not adequately account for physiological mechanisms underlying the development of the various CVD risk factor components. The study sample derives from a basically healthy study population, minimizing the likelihood that girls with EM had a genetic or endocrine disorder.

In conclusion, girls reporting menarche at an earlier than average age are more likely to exhibit adverse changes during adolescence in insulin, blood pressure, lipids, and adiposity during adolescence than their later maturing counterparts. These chronic disease risk factors have been shown to track from childhood to young adulthood and may foreshadow adult disease risk. Although age at menarche is not modifiable, it is important that parents and children are aware that EM may convey more adverse changes in CVD risk factors than average or late menarche. Our results suggest that early maturing girls may need additional diet and physical activity counseling compared with later maturing girls. Earlier ascertainment of disease risk may lead to primary disease prevention or the postponement of subclinical disease progression. Therefore, monitoring early maturing girls for CVD risk factors may be an effective and beneficial disease prevention practice during adolescence.


   Footnotes
 
This work was supported by the National Institutes of Health under Ruth L. Kirschstein National Research Service Award F32-DK064482 from the National Institute of Diabetes and Digestive and Kidney Diseases and Award R01-HD12252 from the National Institute of Child Health and Human Development. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the National Institutes of Health.

First Published Online February 22, 2005

Abbreviations: AC, Abdominal circumference; AM, average menarche; BMI, body mass index; CVD, cardiovascular disease; DBP, diastolic blood pressure; EM, early menarche; FFM, fat-free mass; GIR, glucose-insulin ratio; HDL, high density lipoprotein cholesterol; LDL, low density lipoprotein cholesterol; LM, late menarche; PBF, percent body fat; SBP, systolic blood pressure; TBF, total body fat mass; TC, total cholesterol; TG, triglycerides.

Received October 18, 2004.

Accepted February 9, 2005.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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