Abstract
Introduction. Early pubertal onset among girls has been associated with cardiovascular disease (CVD) risk factors. We examined whether timing of peak height velocity (PHV), an early marker of maturity, was associated with CVD mortality.
Materials and methods. We analysed 973 Icelandic women, born 1921–1935, with annual childhood growth measures from ages 8–13 years, recruited into the longitudinal Reykjavik study 1968–1991. CVD deaths from recruitment to December 2009 were recorded.
Results. Eighty-six women died from CVD, 42 deaths from coronary heart disease (CHD). Compared to girls with PHV after age 12, girls with PHV < 11 years and between 11 and 12 years had greater risk of CVD mortality, hazard ratio 1.87 (95% confidence interval 1.07–3.26, P = 0.028) and 2.56 (1.52–4.31, P < 0.001), respectively. Comparable associations were observed with CHD cases 2.27 (1.17–4.44, P = 0.016) as well as non-CHD CVD cases 2.21 (1.17–4.19, P = 0.015) when comparing girls with PHV after versus prior to age 12. Timing of PHV was not associated with traditional CVD risk factors in mid-life including body mass index and adverse lipid profiles or with all-cause mortality.
Discussion. Earlier timing of PHV in girls may increase the lifetime risk of CVD mortality and may be an important determinant for later cardiovascular health.
Key messages
In this Icelandic cohort of women, reaching peak height velocity prior to age 12 was associated with increased risk of cardiovascular disease mortality.
The association between peak height velocity and cardiovascular disease mortality was independent of mid-life adult body mass index and traditional risk factors.
Timing of peak height velocity, a pubertal event that occurs prior to age at menarche among girls, may be an important determinant for later cardiovascular health.
Introduction
Cardiovascular disease (CVD) continues to be the leading cause of death worldwide. Women tend to have different CVD risk profiles compared to men (Citation1,Citation2), and there is a growing need to provide risk assessment to identify factors that specifically impact women.
Early menarche has been associated with risk factors for CVD such as high blood pressure and elevated plasma lipids at adult age (Citation3,Citation4). Recent reports also suggest an inverse relationship with menarcheal age and adult CVD mortality (Citation5,Citation6). However, previous studies investigating puberty in girls and later disease risk have largely relied on retrospective self-reported age at menarche (Citation3–8). Although the use of recalled menarcheal age has been somewhat validated, the reliability of such retrospective methods vary greatly depending on characteristics of the population including age at recall and education (Citation9).
Peak height velocity (PHV) is a pubertal event achieved prior to menarche (Citation10,Citation11) and has been used as a marker for early development (Citation12). To our knowledge, the timing of PHV and its association with CVD mortality has not been previously investigated. While childhood body mass index (BMI) has been linked to coronary heart disease (CHD) (Citation13), the influence of pre-pubertal height acceleration itself on later disease risk has been less well examined. Furthermore, few studies have been able to take into account the simultaneous influence of mid-life BMI and conventional CVD risk factors.
As early onset of puberty among girls is an ongoing concern due to its associations with adverse health outcomes (Citation14), it is of interest to determine whether timing of height acceleration among girls can provide insight into cardiometabolic risk markers and CVD mortality in adulthood. To achieve this aim, we utilized childhood growth measures gathered from school health records to examine the association between age at PHV among girls and mortality from CVD, including CHD, in adulthood.
Materials and methods
The study population
The longitudinal Reykjavik Study was initiated by the Icelandic Heart Association in 1967 to assess and manage cardiovascular diseases in Iceland (Citation15). In this analysis, we studied a sample of women who were born in Reykjavik and attended the two main schools in Reykjavik where childhood growth data were also collected. The source data for this paper consist of 4601 subjects born between 1914 and 1935 and who resided in Reykjavik when recruited into the study from 1967 to 1991.
Annual recording of height and weight measures began in two main schools in Reykjavik in 1929 for children 8 years of age and older (birth year ≥ 1921). There were 781 subjects born prior to 1921, and 1699 subjects lacked school health records due to migration as not all subjects attended the main schools, leaving us with 2120 participants available for analysis (Citation16). Girls enter puberty, on average, 2 years earlier than boys (Citation17). In this cohort, childhood growth measures were recorded annually from ages 8 to 13 years. For this reason, the 1085 men in the cohort were excluded from the analysis because pubertal timing would not be identifiable based on the growth data we had available. The remaining sample size of 1035 women was further narrowed as PHV could not be accurately identified from growth measures (n = 62). Thus, the final sample size was 973 women.
Comparisons between the women in the source cohort who entered the study versus those who did not (n = 1253) revealed no indication that adult anthropometrics or markers for CVD differed markedly—adult height (165.2 versus 164.7 cm), total cholesterol (6.3 versus 6.3 mmol/L), serum triglycerides (1.1 versus 1.1 mmol/L), fasting glucose (4.4 versus 4.4 mmol/L), systolic blood pressure (129 versus 128 mmHg), and diastolic blood pressure (82 versus 81 mmHg). Informed consent was obtained from all participants, and the study received approval from the Icelandic National Bioethics Committee and the Data Protection Commission.
Collection of birth and growth measures
Birth weight was recorded to the nearest ± 50 g, and birth length from crown to heel (in cm) was obtained from midwives’ birth records stored in the National Archives of Iceland. Childhood growth measures from ages 8 to 13 were recorded in school health records at regular yearly intervals beginning in 1929 at two main schools in Reykjavik. At each yearly exam, the child's height and weight were recorded along with the year and month of measurement. On average, there were 5.5 height measures available per subject from ages 8 to 13 years, with 92% of the cohort having 5 or more measurements.
Timing of peak height velocity
From the growth measures which were collected yearly from ages 8 to 13 in two main Reykjavik schools, height velocity was defined as difference in height between two consecutive annual measurements divided by the time between the two measurements (∆cm/∆time). The changes in height were visually assessed for each participant by two independent reviewers. The maximum height acceleration after 8 years of age was identified as PHV (Citation12) if it was followed by a clear increase in height velocity from the previous year (if after age 8) followed by at least a 1 cm/y decrease the next year with a consistent decrease in height velocity at the subsequent years. If the greatest height acceleration occurred at the measurement taken between 12 and 13 years or there was no marked increase in height velocity, the women were categorized as having late PHV (n = 476). PHV prior to age 12 was identifiable in 497 women (51%), of which one-half (n = 248) had clearly reached PHV prior to 11 years of age (early) and the second half (n = 249) between ages 11 and 12 (middle), leading to the categories used in our analyses (see Supplementary Figure 1 available online at http://informahealthcare.com/doi/abs/10.3109/07853890.2013.852347).
Anthropometrics and blood measures at adult age
Methods on data collection from the Reykjavik Study have been previously described in detail (Citation15). In brief, participants were randomly selected through the National Register and invited by letter or telephone to the Heart Preventive Clinic in Reykjavik to complete a medical examination.
The women in this cohort were recruited between 1968 and 1991, and the mean age of study participants at examination was 51 years (± 6, range 36–65 years). Each participant's height was recorded to the nearest 0.5 cm and weight to the nearest 100 g, without shoes and in light undergarments. Subjects were instructed to consume no food or drink after 10 pm the night prior to the exam. Fasting blood samples and blood pressure after a 5-minute rest in a sitting position were collected by trained nurses. Skinfold measures were collected at two areas, triceps and subscapular, with calibrated callipers to the nearest 1.0 mm (Citation18). Information on medical history, family history, use of medication, and smoking habits was assessed by a standardized health questionnaire completed by the participant and verified by study personnel.
CVD and CHD mortality
The date and cause of all deaths in the cohort were obtained through linkages with the Icelandic Statistical Bureau. Death from any cause and fatal cardiovascular deaths, including CHD and non-CHD, that occurred from the time of recruitment starting from 1968 in this cohort to 31 December 2009 were considered. Death certificates were reviewed and coded by an official government pathologist (Citation19). Death from CVD or CHD was ascertained if death certificates included the following International Classification of Diseases: code 420 (1967–1970, 7th revision), codes 410–413 (1971–1980, 8th revision), codes 410–414 (1981–2009, 9th revision), and codes I20–I25 (2010, 10th revision).
Statistical analysis
The median, mean ± SD, or proportion was used to describe participant characteristics. The associations between variables were evaluated using t tests and chi-square for trend statistics. Cox regression analyses were used to estimate the hazard ratios (HR) and 95% confidence intervals (CI) for the association between age at PHV and CVD, CHD and non-CHD CVD mortality, as well as all-cause mortality. The underlying time-scale was time from study recruitment to fatal CVD event or until 31 December 2009, whichever came first. PHV was categorized as early (prior to age 11), middle (between ages 11 and 12), and late (after age 12). PHV after 12 years of age was used as the reference category.
Due to the low number of cases, analyses for CHD and non-CHD CVD mortality were performed with two categories comparing girls with PHV prior to versus after age 12. Age-adjusted analyses were performed along with further variable adjustments for birth year (dichotomous 3-year intervals from 1921 to 1935), maternal parity, previous and current smoking (dichotomous), age at clinical examination, total cholesterol, systolic blood pressure, and familial hypertension, and additionally for birth weight, BMI at age 8, and mid-life adult BMI. We used SPSS version 20.0 (IBM Corp., NY, USA) for all statistical analyses. The significance level was P < 0.05, two-sided.
Results
The median height gain of girls achieving PHV in the early (< 11 years) and middle (between 11 and 12 years) groups was 7.9 and 8.2 cm/y, respectively (). Among the girls in the late PHV group, there was a trend toward increasing height velocity, median 7.2 cm/y between the ages of 12 and 13 years, but the velocity was lower in comparison to girls with earlier PHV as expected. This also indicates a combination of girls who had reached PHV between the ages of 12 and 13 along with those who had not.
Table I. Median values for height and height velocities from ages 8 to 13 by timing of peak height velocity.
Characteristics of the participants in mid-life adulthood are presented in by PHV category. Differences in age, age at mortality from CVD, and anthropometric measures in adulthood were negligible between the PHV groups, although the mean BMI and proportion of obese women were higher in the middle PHV category (11 to 12 years). At mid-life, though the trends were insignificant, women in the middle PHV category had higher uric acid concentrations, while those in the earliest PHV category had lower diastolic blood pressure and a greater percentage used pain medication.
Table II. Anthropometrics and cardiometabolic risk factors at mid-life adulthood, mean ± SD or per cent, by timing of peak height velocity.
At the end of 2009, there were 348 total deaths in the cohort. Eighty-six women died from CVD, of which 42 were from CHD. After full multivariate adjustment (), compared to girls with late PHV, girls with early and middle PHV were at greater risk of overall CVD mortality with corresponding HRs of 1.87 (1.07–3.26, P = 0.028) and 2.56 (1.52–4.31, P < 0.001). There were comparable associations with CHD mortality when evaluating girls with PHV after versus prior to 12 years of age, HR 2.27 (1.17–4.44, P = 0.016) as well as for non-CHD CVD mortality 2.21 (1.17–4.19, P = 0.015). These associations remained stable after adjustment for both childhood BMI at age 8 and mid-life adult BMI. Timing of PHV was not associated with all-cause mortality.
Table III. Hazard ratios for CVD, non-CHD CVD, and CHD mortality by category of peak height velocity.
Discussion
In this current analysis of 973 Icelandic women, we found that earlier PHV, i.e. prior to 12 years of age, was associated with higher rate of death from CVD but not all-cause mortality. Comparable associations were observed with CHD and non-CHD CVD mortality. Variations in our findings by cause of death suggest distinct processes are involved with respect to the influence of childhood height acceleration. Furthermore, this association did not appear to be fully mediated through childhood BMI or well-established risk factors for CVD in mid-life such as total cholesterol, systolic blood pressure, or BMI.
There have been no previous studies evaluating PHV among girls and later risk of disease, so we compare our findings to reports on early age at menarche. Large-scale epidemiological studies support our main finding that early maturity and CVD mortality are linked independent of adult body size (Citation5,Citation6). The European EPIC-Norfolk study of Caucasian women found that menarche before age 12 was associated with increased risk of CVD mortality, HR 1.28 (1.02–1.24), which was only partly mediated by increased adult adiposity (Citation5). In a population of Singaporean Chinese women, early menarche was associated with CVD and CHD mortality with corresponding HRs of 1.17 (1.07–1.27) and 1.23 (1.06–1.43) after adjustment for adult BMI (Citation6). Both studies used retrospective recall of menarche and the age category prior to 12 years to indicate early maturation. It is likely that these early-maturing girls were experiencing PHV prior to age 12, which would be similar to the girls in the early PHV group in our cohort. The greater risk estimates in our cohort may imply that PHV is more strongly related to CVD mortality compared with age at menarche. However, given our modest number of cases and the broad confidence intervals observed in our analyses, our findings may be compatible with a smaller hazard ratio.
Associations between age at menarche and cardiometabolic risk factors have been more ambiguous. Findings from the Fels Longitudinal Study and the Bogalusa Heart Study showed that women with early menarche exhibited higher blood pressure (Citation20) and a greater prevalence of syndrome X (Citation21) in early adulthood. In a Finnish cohort, using standardized height growth as a proxy for early puberty, subjects with early pubertal timing had increased blood pressure, higher BMI, and shorter stature in adulthood compared to individuals who experienced puberty later (Citation7). Other cohorts have found no connection between early menarche and adult blood pressure or diabetes (Citation22,Citation23). In our cohort we did not find marked differences by timing of PHV for select CVD risk factors, and adjustments for these variables strengthened the associations observed. We also found no differences between timing of PHV and adult height which is in line with existing reports on pubertal growth (Citation17,Citation24). Adverse CVD risk factors did not appear to influence the association between childhood height velocity and CVD death, at least at mid-life. However, we note that these factors were measured at only one time point and likely contributed to the outcomes we observe.
While PHV and onset of menarche are both downstream events of initial pubertal onset, in populations where childhood growth measures are available, identification of PHV may be a useful objective marker for CVD risk similar to age at menarche (Citation4). It is probable that earlier PHV leads to earlier onset of menarche, and the timing of PHV may be the growth phase during which mechanisms are triggered that accelerate both height gain and simultaneously contribute to adult metabolic disorders (Citation7). Whether this occurs due to fluctuations in sex hormones such as estrogen or changes in adiposity and/or adverse blood lipid profiles needs to be elucidated and is an area where further follow-up is required.
Other environmental exposures, e.g. organic pollutants, have also been implicated in progressing onset of puberty (Citation25). All participants in this current analysis were born in Reykjavik and went to school and were living there as adults when recruited into the study. Although not a completely isolated environment, the women would have been exposed to similar external environments. Immigration into the country was also very minimal during this period, and different racial backgrounds would not be a source of bias. Early maturation among current youth has also been associated with unhealthy behaviours such as smoking which continue into adulthood (Citation26). Associations remained significant after adjustments for former and current smoking, suggesting that it was not a major confounder in our analyses.
Additional factors not controlled for might be involved in the outcomes we observed. For example, age at menopause is also associated with risk of CVD (Citation27). In women of Northern European descent, the average age at menopause is between 50 and 51 years (Citation28). When we truncated our analyses to women ≤ 50 years of age as an estimate of women who had likely not entered menopause, the risk estimates for the association between PHV (late versus early) and total CVD mortality after multivariate adjustment went from 1.87 (1.07–3.26) to 2.11 (0.81–5.52). The central risk estimate does not change dramatically, and the wider confidence intervals can be attributed to the lower numbers of cases (30 versus 86 CVD deaths in the total cohort). Although menopause may have had some effect on later CVD death, we still find an increased risk of CVD mortality among women who likely had not entered menopause.
In recent years, the role of the adipocyte-derived hormone leptin on pubertal timing has been of growing interest. Animal studies have shown that inadequate energy intake in pubertal rats halts the development of reproductive organs (Citation29), and in leptin-deficient mice introduction of the hormone induces puberty (Citation30). As leptin is known to have atherogenic effects (Citation31), earlier exposure to higher leptin levels could be an unexplored mechanism for the increased CVD mortality seen among the women who had earlier PHV.
There are some limitations in the present study. Growth measures after 13 years of age were not available for analyses, and thus we were unable to determine the timing of PHV if it occurred after this age. Measurement error is also a possibility; however, the mean childhood height measures in our cohort were found to be a fair representation of school children in Iceland during this period when compared to reference data for all public schools in Reykjavik (Citation32). Furthermore, each child's height was clinically measured in regular yearly intervals by a trained health professional and did not rely on self-reported information, making it possible to compare with relative accuracy girls with early PHV to those with PHV after age 12. Longitudinal growth studies have shown that the PHV in average-growing girls is 8.1 cm/y (Citation33). A more recent study comparing average PHV among American girls reported the average to be 8.3 cm/y and not different from British girls (Citation17). These numbers are consistent with the median height velocity in our cohort in the early and middle PHV categories. The original design for the Reykjavik Study (1968–1991) did not include data on age at menarche. To truly determine if PHV is independently associated with CVD mortality it is essential to compare it alongside menarche data which is an important area for future studies.
We also acknowledge that the number of CHD and non-CHD CVD cases is modest, yet we still observe similar risk estimates in these categories despite the limited sample size. The lack of a dose-response when evaluating all CVD deaths could be attributed to both a lower number of cases and to the fact that almost 50% of our cohort were in the PHV category > 12 years of age. The change in risk likely could not be captured with the growth data we had available and may be observed if growth was collected beyond 13 years of age.
Conclusions
Our findings suggest earlier PHV can increase the lifetime risk of CVD mortality independent of BMI at age 8, mid-life adult BMI, and CVD risk factors. In general, there appears to be no beneficial effect of early maturity on later health. Early height acceleration, even among normal-weight children, is an easily tracked measurement, and by closely monitoring pre-pubertal and adolescent growth we may be able to recognize growth patterns associated with later disease and identify appropriate timing of clinical interventions.
Supplementary Figure 1
Download PDF (135.1 KB)Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
This work was supported by the University of Iceland Research Fund and Landspitali National University Hospital Research Fund. The sponsors had no role in the design or conduct of the study.
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