The Individual Relationship between Pubertal Growth and Physical Changes of Puberty in Healthy Adolescents

Abstract

Introduction

In healthy adolescents, there is significant interindividual variation in the dynamics of pubertal growth and in the timing and progression of physical changes of puberty. Our aim was to explore the relationship between pubertal growth and pubertal maturation through an analysis of data from a longitudinal growth study.

Methods

The Edinburgh growth study included healthy children born between 1972 and 1976 with a birth weight of >2.5 kg. Anthropometric measurements and Tanner staging were undertaken twice a year. Total pubertal growth (TPG) was quantified using the QEPS growth model, which generates an individual growth curve from birth length to adult height (AH).

Results

A total of 157 adolescents were included in analysis (89 boys, 68 girls). In girls, later age at reaching all the stages of breast maturation (B2–B5) was correlated with smaller TPG. Correlation coefficient between B3 and TPG was −0.64, p < 0.01. However, there was no correlation with AH (coefficient 0.15, p = 0.24). In boys, later age at reaching the later stages of external genitalia maturation (G4–G5) was correlated with smaller TPG. G4 was negatively correlated with TPG (−0.24, p < 0.04) but not with AH (0.02, p = 0.86).

Conclusion

We found that the magnitude of the pubertal growth spurt was linked with the age at reaching Tanner landmarks of puberty in girls and boys; however, there was no association between the timing of these landmarks and AH. This new knowledge can provide reassurance for healthy children that the normal variation of pubertal timing does not have a significant influence on expected AH.

Plain Language Summary

Puberty describes the biological process of a child turning into a young adult, and it is characterised by a growth spurt and physical changes including breast development (maturation) in girls and testicular maturation in boys. There is wide variation in the growth spurt and timings of the physical changes in normal puberty. We investigated if the dynamics of the growth spurt was related to the timings of the physical changes at an individual level. We analysed the Edinburgh growth study, a study that followed the growth of healthy children from birth to adulthood and performed regular clinic assessments as their bodies matured into adults. A mathematical model was used to generate individual growth curves. We analysed data from 157 individuals (89 boys, 68 girls). In girls, older age at reaching all stages of breast maturation was associated with a smaller pubertal growth spurt. However, there was no impact on adult height. In boys, older age at reaching later stages of testicular maturation was associated with a smaller pubertal growth spurt but this did not affect adult height. Adult height was not affected despite patterns between pubertal growth and timings of physical changes of puberty. This is reassuring that while the journey of puberty looks different for every healthy child, they all reach the same destination in their growth.

Introduction

Puberty is a complex biological process that leads to maturation of the reproductive system in humans, denoting the transition from childhood to adulthood. Pubertal development is multifactorial, a combination of genetic, metabolic including prepubertal body composition and social-environmental factors including race [1, 2]. Puberty involves physical, emotional, and hormonal changes. Physical changes include the maturation of secondary sexual characteristics, change in body composition, and a period of acceleration followed by deceleration in skeletal growth (the pubertal growth spurt).

Longitudinal growth studies have shown that puberty involves a predictable pattern of events (physical changes) and peak height velocity (PHV) during puberty can be rapid but these studies, mainly due to small numbers of participants, have mostly presented data as a group or in subgroups. Previously, the PHV of the pubertal growth spurt has been studied compared to the timeline of gonadarche in boys and thelarche in girls [3–6]. However, the relationship between the dynamics of the pubertal growth spurt and the dynamics of the physical changes of puberty is not well understood. Few studies have studied pubertal growth and pubertal maturation in the same population, and even fewer studies have used a growth model to quantify pubertal growth. There is significant interindividual variation in age of onset and progression of pubertal maturation and variation in the shape of the pubertal growth spurt among healthy individuals.

Aims

We aimed to study whether the tempo and dynamics of the pubertal growth spurt correlate with the timing and progression of the physical changes of puberty at an individual level.

• 1.Is the age of onset and progression of the physical changes of puberty associated with the duration of pubertal growth and total pubertal growth (TPG)?
• 2.Is the age of onset and progression of pubertal maturation associated with adult height (AH) attained?

Methods

We performed a secondary analysis of the control group in the Edinburgh growth study. The Edinburgh growth study was a longitudinal study of healthy children (control group) established to make a comparison with children having sex chromosomal aneuploidy. Ethical approval was obtained for the original study as detailed here [7, 8]. Participants in the control group were children born as singletons in Edinburgh between 1972 and 1976 with a birth weight of >2.5 kg. Two male infants were further recruited in 1978. Chromosome karyotype 46,XY or 46,XX was confirmed in all participants. None had chronic disease or lived in social deprivation.

Anthropometric measurements and, when appropriate, assessment of the maturation of secondary sexual characteristics were undertaken by a specially trained team twice a year (around their birthday and at midyear point) from birth until the age they reached AH. The principal investigator was personally trained by Professor James Tanner. The principal investigator trained the other three paediatricians in the team. The equipment and techniques used in the Edinburgh study were identical to the ones used in the Harpenden Growth Study bar one difference: assessment of breast, male genitalia, and pubic hair was from clinical assessment (during 6-monthly clinic reviews), not from photographs as in the Harpenden study [3, 4]. Tanner landmarks of puberty were recorded at age of clinical assessment, but the transition between landmarks may have occurred up to 5 months prior as clinics were 6-monthly. Onset of pubertal maturation was denoted as age at reaching Tanner stage B2 (breast) in girls and age at reaching Tanner stage G2 (external genitalia) in boys.

The QEPS growth model (shown in Fig. 1) generates an individual growth curve from birth length to AH, providing individual estimates with confidence intervals of defined pubertal growth (P-function) in relation to total growth during puberty [9, 10]. Growth is modelled by incorporating quadratic function (the continuous growth from foetal life to adulthood), exponential function (the decline of foetal/infancy growth), pubertal function (pubertal growth spurt), and stop function (declining growth into adulthood). The QEPS model has previously been validated in the Edinburgh cohort [11].

Fig. 1.

The QEPS growth model (Holmgren et al. [11], p147). Left: The graph shows the four mathematical functions that combine to describe growth (total gain in height) from foetal life to adulthood (18 years). t0 denotes 6 weeks postconception, and B denotes birth. The three vertical arrows indicate the fitted individual height-scale parameters: Eheightscale (green), Qheightscale (blue), and Pheightscale (red). The two horizontal arrows indicate the time-scale parameters: Etimescale (green) and Ptimescale (red). The red dot indicates the location of mid puberty, AgeP50. Right: Total height and height velocity estimated by the QEPS model are shown for an individual. Onset, AgeP5, is age at which 5% of the P-function growth is reached. Mid puberty, AgeP50, is age at which 50% of the P-function growth is reached. Age at PHV, AgeTPHV, is when the total height function T from the QEPS model is reached. End of pubertal growth, AgeP95, is age at which 95% of the P-function growth is reached and marked with vertical lines. The duration of puberty is shown by the red horizontal line. The total pubertal height gain (TPG) is shown as the growth from AgeP5 to AgeP95 from the total growth curve (TgainP5–95). The specific pubertal function height gain is Pmax.

As depicted in Figure 1, the model allows detailed examination of pubertal growth by separating specific pubertal function growth (Pmax) from ongoing basic growth (QE-function). Onset of pubertal growth was defined as AgeP5 (when 5% of Pmax had been achieved). The middle of pubertal growth was measured in two ways: firstly, the age at which 50% of Pmax had been achieved (AgeP50), and secondly, the age at PHV of TPG (AgeTPHV). Age at the end of pubertal growth period was AgeP95 (age at which 95% of Pmax had been achieved). Duration of pubertal growth was defined as AgeP95 – AgeP5. TPG incorporates the height gain (cm) from Pmax and QE-function within the pubertal growth period. AH was available from the original dataset. TPG contribution to AH (%) was calculated to account for interindividual variation in height prior to onset of puberty. QEmax was the combined gain in AH (cm) due to Q-function and E-function growth.

Children were excluded if there was a lack of measurements in childhood or uncertainty when AH was reached. Descriptive statistical analysis was performed using GraphPad Prism version 10 (GraphPad Software, Boston, MA, USA). Data were inspected for skewness (visually and computed) with no significant skewness seen (defined as <−1 or >1), so mean and standard deviation were presented. The paired t test was used to study the association between two continuous variables from the same individual. Pearson’s correlation coefficient was used to measure linear correlation between two continuous variables. All statistics were two-sided, and results were considered statistically significant if p < 0.05.

Results

This analysis included a total of 157 children (89 males, 68 females) with complete longitudinal data. The chronological Tanner landmarks of puberty in relation to the beginning, middle, and end of pubertal growth are presented for boys and girls in online supplementary Tables 1 and 2 (for all online suppl. material, see https://doi.org/10.1159/000550225), respectively, compared with the Harpenden Growth Study as a standard. In boys, the onset of pubertal growth (AgeP5) occurred a mean of 0.50 years (SD 0.78) after G2, the first stage of external genitalia maturation (p < 0.01, paired t test). In girls, AgeP5 preceded the first stage of breast maturation (B2) by a mean of 0.76 years (SD 0.91) (p < 0.01, paired t test). Age at G4 had the strongest positive association with AgeP50 in boys (coefficient 0.89, p < 0.01), and age at B3 had the strongest positive association with AgeP50 in girls (coefficient 0.90, p < 0.01) (Fig. 2). Overall, 74.32% (55/74) of boys and 70.77% (46/65) of girls had achieved 50% of pubertal growth around or after G4 and B3, respectively. In the minority 25.68% (19/74) of boys who had passed AgeP50 before reaching G4, AgeP50 occurred at a mean of 3.86 months (range 1.5–8.2) prior. In the 29.23% 19/65 girls who had passed AgeP50 before reaching B3, AgeP50 occurred at a mean of 4.34 months (range 1.24–9.39) prior.

Fig. 2.

The age at which the middle of puberty (AgeP50) occurred in relation to age at reaching Tanner stage G4 in boys (a) and Tanner stage B3 in girls (b). There was a strong positive correlation between age at G4 and AgeP50 (coefficient 0.89, p < 0.01). There was a strong positive correlation between age at B3 and AgeP50 (coefficient 0.90, p < 0.01).

The correlations between ages at onset and progression of gonadarche, thelarche, menarche, and pubarche with the dynamics of pubertal growth are detailed in online supplementary Tables 3 and 4. The number of children by age of pubertal onset is presented in online supplementary Tables 5 and 6. Key findings are discussed below.

Correlation between Gonadarche and Pubertal Growth

The age at reaching the later Tanner stages of gonadarche (G4 and G5) was associated with duration of pubertal maturation and TPG. Age at reaching G4 was positively correlated with duration of pubertal growth (coefficient 0.30, p < 0.01). The older the age at which a boy reached G4, the longer the duration of pubertal growth (Fig. 3a). Mean (SD) duration of pubertal growth was 4.34 years (0.27). Conversely, the age at reaching G4 was negatively correlated with TPG (coefficient −0.24, p < 0.04) and TPG contribution to AH (coefficient −0.27, p = 0.02). The older the age at reaching G4, the smaller the TPG (Fig. 3b) and the smaller the contribution of TPG to AH (Fig. 3c). Mean (SD) TPG was 29.70 cm (3.54), and mean (SD) TPG contribution to AH was 16.71% (1.93). However, there was no correlation between age at G4 and AH (coefficient 0.02, p = 0.86) (Fig. 3d). Mean (SD) AH was 177.8 cm (6.86). Similar correlations were seen between age at reaching G5 and dynamics of pubertal growth. In boys who reached the later stages of gonadarche at an older age, AH was not impacted despite reduced total growth during the pubertal period.

Fig. 3.

Correlation of age at reaching G4 with duration of pubertal growth (a), TPG (b), contribution of TPG to AH (c), and AH (d) in boys.

Ages at reaching the earlier stages of gonadarche (G2 and G3) were not associated with duration nor TPG. However, the age at reaching G2 and G3 was associated with specific pubertal growth (Pmax). Age at G2 was positively correlated with Pmax (coefficient 0.23, p = 0.04). The older the age at which a boy started puberty, the greater the Pmax. Age at G3 also had a similar positive correlation with Pmax (coefficient 0.30, p = 0.01). Mean (SD) Pmax was 17.06 cm (3.40). Mean (SD) Pmax proportion of TPG was 57.16% (7.09). There was no direct correlation between the later stages of gonadarche (G4 and G5) with Pmax.

Age at G2 was negatively correlated with AH (coefficient −0.31, p < 0.01), but there was no correlation between age at G2 and TPG contribution to AH (coefficient −0.12, p = 0.29). There was a negative correlation (coefficient −0.5, p < 0.01) between age at G2 and prepubertal height (QEmax). Age at G3 did not correlate with AH (coefficient −0.03, p = 0.80).

Correlation between Thelarche and Pubertal Growth

The age at reaching all the Tanner stages of thelarche was associated with TPG but not AH. Figure 4 details the associations between age at B3 and the width (duration) and magnitude (TPG) of the pubertal growth spurt. Age at B3 was strongly negatively correlated with TPG and TPG contribution to AH (coefficient −0.64, p < 0.01 and −0.67, p < 0.01, respectively). Mean (SD) TPG was 27.23 cm (3.95), and mean (SD) TPG contribution to AH was 16.57% (2.40). However, there was no correlation between age at B3 and Pmax (coefficient 0.002, p = 0.99) and age at B3 was not correlated with AH (coefficient 0.15, p = 0.24) (Fig. 4d). Mean (SD) Pmax was 13.02 cm (3.16), and mean (SD) AH was 164.4 cm (5.59).

Fig. 4.

Correlation of age at reaching B3 with duration of pubertal growth (a), TPG (b), contribution of TPG to AH (c), and AH (d) in girls.

Only ages at reaching the later stages of breast maturation (B4 and B5) were positively correlated with duration of pubertal growth (coefficients 0.27, p = 0.04 and 0.25, p < 0.04, respectively). In our cohort of girls, 4 (5.9%) started puberty (B2) before 9 years old (range 7.5–8.6 years) and 3 (4.4%) experienced moderately late pubertal onset after 13 years of age (range 13–14.7 years).

Correlation between Menarche and Pubertal Growth

Residual growth related to age at menarche is detailed in online supplementary Table 7. A total of 65/68 (95.6%) girls reached menarche between the age of 11 and 14 years. Two reached menarche aged 10 years, and one reached menarche aged 17 years. Although age at menarche was positively correlated with the duration of pubertal growth (coefficient 0.29, p = 0.01), there was no correlation with Pmax (coefficient 0.04, p = 0.77). Similarly to thelarche, age at menarche was negatively correlated with TPG and contribution of TPG to AH (coefficient −0.61, p < 0.01 and −0.64, p < 0.01, respectively). The older the age at menarche, the smaller the size of the pubertal growth spurt (Fig. 5). However, age at menarche was not correlated with AH (coefficient 0.10, p = 0.40).

Fig. 5.

Correlation of age at menarche with duration of pubertal growth (a), TPG (b), contribution of pubertal growth to AH (c), and AH (d).

Correlation between Pubarche and Pubertal Growth

Age at PH4 and PH5 in boys was negatively correlated with TPG and TPG contribution to AH. However, ages at PH4 and PH5 did not correlate with AH. In girls, ages at reaching all stages of pubarche (PH2–PH5) correlated with TPG and TPG contribution to AH. However, there was no correlation with AH. Delay in reaching the later stages of pubarche in boys and later onset and progression of pubarche in girls were not associated with AH despite correlations with the size of the pubertal growth spurt.

Discussion

We have evaluated the relationship between pubertal growth and the physical changes of puberty at an individual level, and have provided new insights into the correlation between the dynamics and tempo of pubertal growth along with the timing and progression of the physical changes of puberty in healthy adolescents. We found the age at reaching the middle of pubertal maturation (G4 in boys and B3 in girls) was strongly positively correlated with age at reaching the middle of pubertal growth (AgeP50). Variation in onset and progression of pubertal maturation corresponded with patterns of pubertal growth. Age at reaching G4 and G5 in boys and age at all stages of breast maturation (B2–B5) were negatively correlated with TPG. Similarly, older age at menarche was associated with smaller TPG. Apart from age at G2, the age at reaching the other stages of gonadarche was not associated with AH. Neither age at thelarche nor age at menarche were associated with AH.

Although the growth pacemaker is not completely understood, the age at reaching each of the Tanner stages of pubertal maturation does not appear to influence AH attainment in healthy adolescents significantly as the control mechanism appears to balance age at onset of puberty with pubertal growth and other growth pathways to reach AH by a set timepoint. Thus, in routine clinical practice, in the absence of obvious pathology, one can reassure a child they will likely achieve their full growth potential irrespective of the timing of pubertal milestones.

Our data were from a historic longitudinal study with participants born in the early-mid 1970s and thus reaching puberty in the late 1980s and early 1990s. The measurements from this study provide the growth pattern trajectory of current UK charts. There are no more contemporaneous longitudinal studies of pubertal maturation and growth that include AH.

Secular trends indicate earlier onset of puberty, and this is associated with increased prevalence of obesity [12, 13]. There is often clinical concern that children who begin pubertal maturation early or rapidly progressing children may have a truncated growth spurt. Our study explored the intra-individual relationship between total height gain during puberty and the timings of pubertal maturation, which is unlikely to be directly influenced by secular trends. Our findings remain useful to practising paediatricians and paediatric endocrinologists when counselling a healthy child about the variability in normal pubertal maturation and pubertal growth.

The Peak of Pubertal Growth in Relation to Timing of Pubertal Maturation

In our cohort of 89 boys, the middle of pubertal growth occurred within stages G3 and G4, which is in keeping with the Harpenden study, of which only 60/228 had PHV available [3]. Our results are also in agreement with the 1st Zurich longitudinal growth study of 120 boys born between 1954 and 1956, which found 2% had achieved pubertal PHV by G3, 37% by G4, and 90% by G5 [6]. Our results are also in keeping with the longitudinal Barcelona study of 223 Caucasian boys born between 1978 and 1982, which showed PHV occurred between G3 and G4 [5, 14].

In our cohort of 68 girls, the middle of the pubertal growth spurt occurred around or after transition to B3. This is consistent with the Harpenden study (n = 39) and longitudinal Barcelona study (n = 235), which reported PHV occurred between B2 and B3 [4, 5]. The Barcelona study reported B2 occurred 4–6 months after the onset of pubertal growth. B2 occurred a mean (SD) of 0.72 years (0.91) after AgeP5 occurred in the majority of our cohort (82%), but AgeP5 started after B2 in a minority of girls (18%). The longitudinal Zurich study (n = 112) also reported a minority (11%) had not started their pubertal growth spurt prior to B2 [6]. These findings could be partially explained by transient thelarche. Our results show that in the small proportion of girls who experience discordance in thelarche and onset of pubertal growth during normal puberty, AH is not affected.

Our findings are also in keeping with a more recent study of the timing of PHV in relation to timings of pubertal maturation. The National Institute of Child Health and Human Development (NICHD) Study of Early Child and Youth Development began in 1991 and followed healthy children from infancy to 15 years of age [15]. In their cohort of 402 children, they found the majority (58.9%) of boys had achieved PHV by G4 and the majority of girls (69.1%) had achieved PHV by B3. For boys, mean (SD) AgeP50 was 13.99 (0.96) years in our cohort and mean age at PHV was 13.7 (1.4) years in the US cohort. For girls, mean (SD) AgeP50 was 12.14 years (1.21) in our cohort and mean age at PHV was 12.1 years (1.4) in the US cohort [15]. This suggests the age at reaching the middle of pubertal growth has not been noticeably influenced by secular trends indicating earlier onset of puberty.

Age at Reaching Each of the Tanner Stages of Pubertal Maturation Was Not Associated with AH

In our study, the age at reaching each of the Tanner stages of pubertal maturation apart from age at G2 in boys was not associated with AH. Age at G2 was negatively correlated with AH. This could be explained by interindividual variation in height prior to onset of pubertal growth spurt as there was a negative correlation between age at G2 and prepubertal height gain, indicating that children with early age at G2 are relatively taller at AgeP5. However, several previous studies have found a positive correlation between later timing of pubertal growth (onset and peak) and AH [10, 16–18]. As discussed earlier, there is limited literature investigating the relationship between pubertal maturation and pubertal growth and the impact on AH.

Our results are in keeping with the Reus longitudinal study of 135 boys and 116 girls dividing the cohort into subgroups based on age (in years) at onset of B2 (girls) and G2 (boys). They found there was no difference in AH attainment between the groups despite differences noted in the tempo of pubertal growth [19]. Later maturers were taller at onset of puberty in both sexes, because of longer duration of prepubertal growth. They experienced shorter pubertal growth duration and shorter pubertal height gain compared to early maturers.

Our results provide further insight into the dynamics of the pubertal growth in relation to the progression of puberty. In our cohort, age at reaching G4 and G5 in boys and all stages of breast maturation in girls were negatively correlated with TPG. In contrast, age at G2 and G3 was correlated with Pmax. This suggests the body may initially compensate for later onset of puberty with increased specific pubertal growth. In girls, none of the ages at B2–B5 were correlated with Pmax. This could suggest the body may adjust for variation in pubertal growth via different pathways in girls compared with boys.

Moderately early pubertal onset (8–9 years) or moderately late pubertal onset (13–14 years) in healthy girls can cause a degree of consternation about whether they will reach their full growth potential. In our cohort of healthy girls, we had 4 who experienced moderately early pubertal onset (age 7.5–8.6 years) and 3 who experienced moderately late pubertal onset (age 13–14 years). The Reus study compared girls with early-onset puberty, defined as aged between 7.5 and 8.5 years (n = 32) to girls with normal onset puberty, who were divided into four groups based on age at onset of puberty (10–13 years old) [20]. Their study definition of onset of puberty was the age at which B2 was observed and a clear increase in growth visually seen on the growth chart. They found despite girls who started puberty earlier having longer duration of pubertal growth and greater pubertal growth gain, there was no significant difference between the groups and AH exceeded target height in all groups. We defined onset of puberty as age at which B2 was observed alone but our results are in keeping with the Reus study.

Age of Menarche Was Associated with TPG

Older age at menarche was associated with a smaller TPG spurt in our cohort. This negative correlation was also found in a subgroup analysis of the GrowUp₁₉₉₀Gothenberg cohort [21]. However, age at menarche was not associated with AH in our cohort. This was not in keeping with the literature. Recalled age of menarche has been reported to be a predictor of AH [22, 23]. In the GrowUp₁₉₉₀Gothenberg subgroup (n = 793), for each later year of menarche, individuals became approximately 0.84 cm taller [21]. A large US longitudinal study (n = 2,256) also found age of menarche accounted for 1.2–2.4% of the variability of AH [24]. Our cohort size may not have been powered enough to detect a correlation between age at menarche and AH.

Pubarche Stages Were Not Associated with AH

A high correlation between the later stages of pubarche (PH3–5) with the later stages of pubertal growth, the age at PHV and age at the end of pubertal growth, defined as age at maximal deceleration has previously been reported [6]. This was seen in both boys and girls, although correlation was higher in boys. However, they did not report the implications of this on AH. We found age reaching PH4 and PH5 in boys and age reaching all the stages of pubarche (PH2–PH5) in girls were negatively correlated with TPG and its contribution to AH. There was no correlation with AH or Pmax.

Limitations

Limitations of this secondary analysis of longitudinal study include lack of availability of parental height data. This was initially recorded for this cohort, but the data were lost. AH achieved compared with predicted AH would be a valuable future study to understand relationship between the dynamics of puberty and AH in the context of pre-existing genetic factors, prepubertal metabolic and environmental factors.

Our cohort was exclusively Caucasian, and although homogenous populations may have some advantages in controlling for some confounding factors, our findings may have limited applicability to other populations. Whole-genome analysis has shown overlap in genetic loci that influence pubertal timing across populations of different biological ancestries; however, different effect sizes have been described [25].

Considerations for Future Research

This study focussed on the individual tempo of puberty in each child. BMI was not factored into the analysis as only two (1.2%) were obese during the pubertal period. The relationship between pubertal maturation and BMI is not completely understood. Earlier onset of puberty in girls (thelarche) was associated with BMI ≥85th percentile in recent longitudinal US studies [13, 26]. This association with BMI was seen regardless of race/ethnicity [13, 26]. Furthermore, earlier onset of thelarche was associated with increased interval duration to menarche, i.e., a slower tempo of pubertal maturation [27]. In the same study, BMI ≥85th percentile was also inversely associated with menarche. BMI was not associated with earlier pubertal onset in boys compared to girls [26].

However, a Chilean study found BMI was not specifically linked with age at thelarche but thelarche was associated with other markers of adiposity such as higher waist circumference and percentage of fat mass [28]. The authors did report that BMI ≥85th percentile was associated with earlier PHV.

Separate analyses of the mixed methods cross-sectional and longitudinal Danish Copenhagen Puberty study have reported conflicting conclusions. No association between BMI and age at thelarche in girls (n = 89) of the longitudinal study arm was identified [29]. Similarly, no association between BMI and age at gonadarche in boys (n = 90) of the longitudinal study arm was identified. However, an analysis of the combined cross-sectional and longitudinal cohort of boys (n = 730) found an inverse association with gonadarche, pubarche, axillary hair growth, voice break, and testosterone levels [30].

The above-mentioned studies did not examine impact of BMI on AH. Peak BMI in childhood has been found to be inversely associated with pubertal height gain, but AH was similar between overweight/obese and normal weight/underweight children [31, 32]. Further research to delineate the bidirectional relationship between pubertal maturation and increased body adiposity would aid clinicians in counselling adolescents and families about the dynamics of pubertal maturation and growth in the context of increased body adiposity.

Our study only looked at AH in terms of standing height. It would be valuable to look at different components of height in the future such as sitting height, leg length, and bi-iliac width to understand how the body compensates for variation in pubertal growth dynamics to reach AH. It has been reported girls who started their pubertal growth later had longer legs as adults compared to their peers who started pubertal growth 1.5 years earlier, but there was no significant difference in boys [33]. The team divided the cohort into three subgroups to define early vs. late onset of pubertal growth. They found in both sexes that the early subgroups had higher growth velocities during childhood and pre-adolescence to compensate for starting pubertal growth earlier. Future analysis of the relationship between prepubertal growth and pubertal growth at an individual level in our cohort would provide further insight into how the human body’s growth pacemaker works to reach a set height.

Conclusion

We have evaluated the pubertal growth spurt relative to the timings of the physical changes of puberty at an individual level. Among significant interindividual variation in onset and timing of pubertal maturation, we found interesting correlations with patterns in the width (duration) and size (height gain) of the pubertal growth spurt in both boys and girls. However, the variability in progression of pubertal maturation did not have a major impact on AH. This is reassuring for counselling healthy adolescents that while their individual journey of puberty may look different from each other, their AH is unaffected.

Acknowledgments

We are extremely grateful to the late Professor Kerstin Albertsson-Wikland (University of Gothenburg, Sweden) for her expertise and support for this project. We sincerely acknowledge the voluntary participation of the children and parents in the Edinburgh study and their significant contribution to the study of pubertal growth and development.

Statement of Ethics

This was a secondary analysis of data from the control group in the Edinburgh Study of Growth and Development in Children With Sex Chromosome Abnormalities [7]. This retrospective review of patient data did not require ethical approval in accordance with UK NHS Health Research Authority guidelines. Additional informed consent from participants for this secondary analysis was thus not required. The initial study had been supported by the UK Medical Research Council and between 1972 and 1976; chromosomally normal infants were recruited after birth following a personal explanation from the research team and with verbal consent from the mothers. All the mothers had been contacted during pregnancy through a circular informing them of the setting up of a growth and development study. This follow-up study was conducted in accordance with the UK Medical Research Council guidelines for ethical research in children at that time with ongoing voluntary participation from the parents and the children.

Conflict of Interest Statement

The authors declare no conflict of interests.

Funding Sources

This work was conducted as part of G.Y.’s MSc degree at University College London (UCL). G.Y. received financial contributions towards tuition fees from the UK National Institute for Health and Care Research, UCL Academic Careers Office, and UCL Great Ormond Street Institute of Child Health and NHS, England (combined value GBP 12,000). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author Contributions

G.Y. and G.B. conceived the study concept and designed the study with input from A.H. G.B. was a primary investigator of the study used and performed most of the pubertal height measurements. A.F.M.N. ran the QEPS programme on the dataset. G.Y. performed the data analysis with support from A.H. and G.B., and wrote the first draft of the paper. A.H. and G.B. revised the paper for important intellectual content, and all authors approved the final version to be submitted for publication.

Funding Statement

This work was conducted as part of G.Y.’s MSc degree at University College London (UCL). G.Y. received financial contributions towards tuition fees from the UK National Institute for Health and Care Research, UCL Academic Careers Office, and UCL Great Ormond Street Institute of Child Health and NHS, England (combined value GBP 12,000). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Data Availability Statement

All data generated and analysed during this study are included in this article and its supplementary material files. Data are stored in the Wellcome Library archive. Further enquiries can be directed to the corresponding author.