What Happens To Skeletal Growth In Response To The Hormonal Changes Of Puberty?
Body composition during puberty is a marking of metabolic changes that occur during this menstruation of growth and maturation, and, thus, holds cardinal information regarding current and futurity health. During puberty, the main components of trunk limerick (total body fat, lean trunk mass, bone mineral content) all increase, just considerable sexual dimorphism exists. Methods for measuring body composition (eastward.yard. densitometry and dual-energy X-ray absorptiometry) and degree of maturity volition be discussed in this review. Components of body composition prove age-to-age correlations (i.e. 'tracking'), especially from adolescence onwards. Furthermore, adipose tissue is endocrinologically active and is centrally involved in the interaction betwixt adipocytokines, insulin and sex-steroid hormones, and thus influences cardiovascular and metabolic disease processes. In determination, pubertal body composition is important, non just for the cess of contemporaneous nutritional status, merely likewise for being linked directly to the possible onset of chronic affliction later in life and is, therefore, useful for disease risk assessment and intervention early on in life.
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Introduction
During puberty, dramatic hormonal fluctuations as well as a rapid growth in body size occur and are accompanied by marked changes in trunk composition. While body composition tin refer to many dissimilar features and be assessed using different methods, here nosotros focus primarily on a few trunk components, including total torso fatty (TBF) mass, fat-gratis mass (FFM) and bone mineral content (BMC). Other related measures of body composition include percentage body fat, lean body mass (FFM – BMC), bone mineral density and full torso h2o. In addition, torso limerick in other contexts can be considered in terms of the masses of diverse tissues or organs, body cell mass, fat-free extracellular solids, and extracellular h2o, besides every bit past its chemic limerick (e.grand. potassium, nitrogen etc.) [1]. Pubertal development involves the chemical maturation of body tissues, including the corporeality and distribution of adipose tissue, and increases in os mass and fat-free lean tissue mass.
In this review, we will begin by providing an overview of the general cantankerous-sectional changes in body composition in boys and girls during puberty. We will then discuss common measures of torso composition and methods of assessing torso composition and pubertal development. Finally, the importance of trunk composition during puberty will exist considered, including the endocrinological role of adipose tissue, secular increases in adiposity, and the serial interactions between torso composition and the process of maturation.
Patterns of Alter in Trunk Composition during Puberty
There is significant sexual dimorphism in puberty, not only in the timing of pubertal events, but also in body limerick [2, 3, four]. Both sexes experience rapid increases in TBF, although the proportion of body fat increases more than slowly in boys equally a event of a simultaneous rapid increment in FFM [5]. Information from girls in the Fels Longitudinal Written report show that levels of TBF increment at a fairly constant rate from a mean of approximately 5.five kg at viii years of age to about 15 kg at 16 years, after which the rate of increase slows considerably. In boys, there is an increase in TBF from a hateful of approximately 5.0 kg at 8 years to most 11.0 kg at fourteen years, after which TBF falls to approximately nine.0 kg at 16 years and subsequently reaches a plateau. The patterns of pubertal change in males and females for FFM are, to some extent, reversed. In girls, FFM increases until around the age of 15 years, and then remains relatively unchanged. In boys, however, FFM increases steadily between the ages of 8 and 18 years, with a more rapid increment between 12 and 15 years of age.
In that location are significant increases in the energy requirements of children, associated with changes in body limerick. These increases vary, are sex-dependent, and occur at an early on stage of puberty as a result of increases in concrete capacities and energy expenditure [6]. The differences between the sexes that emerge in metabolic rate and physical strength are explained largely by the greater amount of FFM in boys [half-dozen]. Furthermore, the hormonal changes associated with the onset of puberty in boys, such as increased testosterone and growth hormone metabolism, may business relationship for the larger energy expenditure plant in pubertal compared with pre-pubertal boys.
Methods for Measuring Trunk Composition
Methods used to estimate and measure the fat, lean and bone mineral components of body composition range from relatively simple field methods using anthropometrics, such as height and weight, to highly sophisticated approaches requiring specialized laboratories and equipment (e.one thousand. neutron activation). The methods by and large used today include anthropometrics, hydrodensitometry, air deportation plethysmography, dual-energy 10-ray absorptiometry (DXA), bioelectric impedance, deuterium oxide dilution, magnetic resonance imaging (MRI) and computed tomography [1, 7]. The last 2 methods have been used in children and adults and tend to exist well tolerated by both; notwithstanding, the higher radiations doses required for computed tomography brand this method less desirable in some contexts.
Anthropometry
Apart from the basic measures of pinnacle and weight, the introduction of skinfold calipers and other anthropometric equipment in the 1950s allowed for reliable measurement of subcutaneous fat in dissimilar regions of the body, as well every bit the measurement of body widths and circumferences. These measurements tin so be used in population-specific prediction equations to estimate various components of body composition. For example, mid-arm and mid-thigh circumferences can be used to guess muscle mass in the absence of more direct methods. Waist and hip circumferences can exist used to narrate the distribution of body fatty on the torso – an important contained risk factor for centre disease and diabetes mellitus. Anthropometric methods, as measures of subcutaneous fatty and rough estimates of muscle mass, are, nonetheless, indirect in their ability to approximate total torso composition. In add-on, considerable training to take measurements likewise every bit to monitor patients is required to achieve sufficiently high reliability for scientific research purposes.
Torso mass index (BMI) is easy to obtain and is therefore a commonly used index of body limerick (adiposity). It is defined as weight in kilograms divided by the square of stature (standing height) in metres. BMI is often used to determine overweight and obesity in the clinical surround, unremarkably by comparison of an private to age- and sex-specific percentiles from a reference population [viii]. In this context, a variety of recommendations have been made, such as using specific percentiles to define overweight and obesity [nine]or setting cut-off values at childhood percentiles that represent to the adult values for overweight and obesity – values that are known to be related to morbidity and mortality [x]. The adult BMI values that characterize that individuals are overweight and obese, 25 and 30 kg/mtwo, respectively, correspond to the 80th and 95th percentiles of the United states National Heart for Wellness Statistics reference values for xviii-year-one-time children [11, 12]. The US Centers for Affliction Control and Prevention accept recently published new reference childhood growth charts for BMI [8, 13, xiv, fifteen].
Although the BMI values are widely applied to both children and adults, there are serious limitations regarding the employ of BMI every bit an index of adiposity in children [xvi]. BMI in adults is largely contained of stature; information technology is not, however, independent of stature in children and is quite sensitive to torso build [16]. For case, children and youths with undersized legs for their pinnacle will have higher BMI values compared with children with longer leg lengths relative to their height. Furthermore, despite high positive correlations betwixt measures of BMI and adiposity, such as TBF and percent body fat across all age groups, BMI also has a strong positive correlation with FFM in children [5, 17, xviii, xix]. BMI only has low-to-moderate sensitivity in identifying children with backlog TBF or percentage body fatty, indicating that the use of BMI to identify children who are overweight is just poor-to-fair [20, 21].
Densitometry
Hydrodensitometry was adult in the early 1960s and uses the difference betwixt torso weight measured on dry out state and during total h2o immersion to approximate full body density. Measurement of residuum lung volume is necessary to adjust for the buoyancy caused past unexpelled air remaining in the lungs during the test. Total body density, and the known constant density of adipose tissue, may then be used to calculate TBF, FFM and per centum torso fatty. Hydrodensitometry has remained the 'gold standard' of body composition estimation since the 1960s, because of its ability to measure full torso density accurately and precisely. Limitations of hydrodensitometry, all the same, include cumbersome equipment (i.eastward. a water tank), participant performance and discomfort (i.eastward. water immersion) and a restriction to a ii-component view of body limerick (fat mass and FFM) [vii].
Air deportation plethysmography measures changes in gas pressure level when a patient enters a closed chamber, resulting in the deportation of air [22, 23]. The volume of air displaced is directly related to the total body volume of the patient, allowing for an estimation of total trunk density, via the measurement of body mass. This method requires adjustments for torso temperature, body area and the volume of air exhaled during the exam. The resulting full body density estimate can be used to calculate pct body fat, TBF and FFM.
Dual-Energy 10-Ray Absorptiometry
DXA, which has widespread utilize in the clinical diagnosis of osteoporosis, uses low-dose radiation to distinguish soft tissue from bone and density variation within soft tissues, and provides estimates of TBF, FFM, lean body mass, BMC, per centum body fatty and bone mineral density. Interpretation of DXA data in children requires consideration of bone size, stage of pubertal development, skeletal maturation, ethnicity and body composition [24]. When boosted subcomponents of the FFM can exist measured, as in the example of bone mass from DXA, they can also be used in conjunction with TBF from hydrodensitometry to generate multi-compartment trunk limerick models.
Other Methods for Measuring Body Limerick
Bioelectrical impedance assay (BIA) uses tissue resistance to a small electrical charge to estimate total body water and thereby estimates FFM [25]. Deuterium oxide dilution also estimates total torso water and, therefore, FFM, simply does so more accurately than BIA. Whole body potassium counters detect the natural radioisotope twoscoreK, providing a mensurate of musculus mass [26]. Finally, methods such as in vivo neutron activation, computed tomography and MRI can provide chemical and spatial models of torso composition. Computed tomography and MRI tin can mensurate intra-abdominal adipose tissue, a metabolically agile fat component shown to be strongly associated with coronary eye disease and diabetes mellitus in adults [27, 28, 29].
Measures of Maturation and Puberty
The main methodological problems in research on puberty are in determining when information technology begins, how it progresses and how information technology should be measured. Mutual measures of maturation include sexual maturation indicators (due east.thousand. Tanner stages and age at menarche), measures of bone growth and epiphyseal fusion (east.g. skeletal age assessment), and landmarks of concrete growth (eastward.thousand. age at peak pinnacle velocity [PHV]).
Sexual Maturation
Tanner stages of sexual maturation are based on pubic hair development for boys and girls, breast development for girls and genital development for boys. The stages progress from pre-puberty (stage 1), through puberty (stages two–4) to post-puberty (stage five). The median age at onset of stage 2 (the beginning of puberty) varies depending on the maturity characteristic and sex activity of the child. For example, for children in the USA, the median age at onset of stage 2 in boys is x.03 years for genital evolution and xi.98 years for pubic pilus development [thirty]. The corresponding median age for onset of stage ii in girls is ten.38 years for chest evolution and 10.57 years for pubic hair evolution [30]. The variation in the age of onset between the two indicators for boys and girls makes the definition of puberty using Tanner stages difficult. Age at menarche is also a pubertal landmark in girls and in that location is considerable population variation in the age at onset. The current average age at onset for girls in the USA is 12.43 years, with the ages at onset of menarche for Caucasian, African-American and Mexican-American girls being 12.55, 12.06 and 12.25 years, respectively [31].
Skeletal Maturation
The skeletal age of an individual tin be assessed using radiographs of the hand and wrist, or the knee. The Fels method for skeletal age cess of the manus and wrist [32]uses grades adamant for degree of bone ossification, shape, and fusion of the carpals, epiphyses of the metacarpals, and the phalanges of digits I, Three and V. The Fels method is widely used in a variety of ongoing pharmaceutical trials involving children in the Usa and is also beingness used in a genetic epidemiological study of skeletal maturation [33]. Relative skeletal age (i.east. skeletal age – chronological age) can exist used every bit a measure of the degree to which an individual is skeletally avant-garde or delayed for their historic period. Skeletal maturation is associated with body composition and tin can be used to identify boring- and fast-maturing children.
Growth and Maturation
Measurements of growth in stature tin also serve as indicators of maturation. When long-term series information are available for an private, a triple logistic model or other statistical models tin can be fitted to the patient'southward serial stature information to calculate parameters of this physical growth curve. The pinnacle velocity bend of a patient is shown in figure ane. Bend parameters can be used to place and quantify growth landmarks, for example, early childhood minimum tiptop velocity (MHV), age at early babyhood MHV, pre-pubertal MHV, historic period at pre-pubertal MHV, PHV and age at PHV.
Fig. 1
Age at PHV is inversely related to the magnitude of PHV in both sexes [34], in that children with an early boyish growth spurt exhibit a higher PHV than children with a later spurt. Boys who have a later growth spurt have been reported to accrue more than os mineral and lean mass and are taller at the age of PHV, compared with boys with earlier growth spurts [34]. Weight and fatty mass, however, practise not appear to differ betwixt maturity groups at the age at PHV in either sex [34]. At a given chronological historic period, children who are more mature tend to be taller and heavier than less mature children. Indeed, children who have a more rapid rate of sexual maturation tend to have a higher risk of obesity in machismo [35, 36].
Importance of Body Composition during Puberty
Monitoring body composition during puberty is of import because many aspects of body limerick during this menstruum are predictive of subsequent measures of these traits in adulthood (i.e. body composition 'tracks') [37, 38]. Adipose tissue, a major component of body composition, is endocrinologically active and has important interactions with sexual activity-steroid hormones [39, xl]. Furthermore, certain aspects of trunk composition and their changes during puberty are risk factors for a diverseness of common, multi-factorial adult diseases, including cardiovascular disease, diabetes mellitus, obesity and osteoporosis [4, viii, 41, 42, 43].
Tracking of Body Limerick from Childhood into Machismo
Series assessment of body composition during puberty allows for the study of changes in values across the unlike age groups. Tracking can be measured by determining the correlation betwixt a trait measured in the aforementioned individual at 2 or more than points in fourth dimension. Tracking of weight is slight-to-moderate from birth to childhood and adolescence [44], while tracking correlations are moderate-to-strong from childhood to adulthood. Correlations of babyhood BMI with adult BMI are low, only increase with historic period during boyhood [37]. For case, amongst children anile 8 to 13 years with a BMI greater than the 95th percentile, 33% of boys and 50% of girls continued to be obese as adults, whereas for adolescents anile 13 to 18 years with a BMI greater than the 95th percentile, l% of males and 66% of females were obese in adulthood [37]. Similarly, birth weight and baby weight have low positive correlations with BMI subsequently in life. These relationships are weak (r <0.xx), and so weight condition in infancy holds picayune predictive value at the individual level. Torso composition components show considerable tracking from childhood onwards. Tracking correlations for TBF and FFM from early childhood into adulthood are low but significant [45, 46], whereas tracking correlations for TBF and FFM from mail service-puberty to adulthood are high [3]. These high tracking correlations from adolescence onwards testify the importance of agreement the changes in body limerick that are related to the timing and progression of puberty because they can predict future body composition.
Adipose Tissue Is Endocrinologically Active
Another important aspect of trunk limerick during puberty is that adipose tissue is agile every bit an endocrine organ. Adipocyte-secreted proteins are produced in response to a variety of changes in metabolic status [39]. Adipocytokines (adipose tissue-derived molecules) include leptin, adiponectin and resistin. These molecules are involved in lipid and lipoprotein metabolism, vascular homeostasis and fibrinolytic role, and some have potent pro- and anti-inflammatory properties [39].
Leptin functions as a regulator of energy residuum [47]by interacting with several neuropeptides to inhibit food intake, and affecting the expenditure of energy. Leptin too appears to be involved in mediating various endocrine mechanisms (due east.grand. onset of puberty, insulin secretion) and is related to disorders including obesity and polycystic ovary syndrome [48, 49]. Leptin is primarily synthesized in adipose tissue, but is too synthesized in the tum, placenta, mammary glands and ovarian follicles, likewise as other organs. Leptin is strongly related to TBF, with blood levels of leptin beingness more strongly correlated with subcutaneous than visceral (intra-abdominal) adipose tissue.
There is a articulate sexual dimorphism in circulating concentrations of leptin, with girls having college serum concentrations of leptin than boys earlier, during and after puberty, even after the greater adiposity in females is taken into business relationship [50]. Pre-pubertal levels of leptin in girls also predict gains in percentage body fatty during puberty [51]. Gonadal steroids are strong candidates for mediators of the sexual dimorphism in leptin concentrations; the state of affairs is, however, more than complex. Circulating leptin concentrations during late puberty are significantly affected by sexual activity, afterwards the furnishings of trunk composition and circulating concentrations of gonadal steroids are accounted for [twoscore]. Thus, the sexual dimorphism may likewise reverberate straight or interactive effects of other sex-related metabolic variables such equally insulin, growth hormone or adipose tissue distribution [twoscore]. Finally, leptin concentration is inversely related to C-reactive protein concentration, a marker of inflammation. The general association of increases in torso fat with increases in inflammation indicates that leptin may have anti-inflammatory properties [52].
Based on a pocket-size, yet detailed, study in children, Roemmich and colleagues [53]showed that pubertal insulin resistance (as measured by the Homeostasis Model Assessment [HOMA]) is associated with body composition. Their results led them to speculate that the accumulation and distribution of fat in the abdominal, visceral, subcutaneous and muscular components of the body may increase insulin resistance during puberty beyond that acquired by TBF. In addition, they speculated that serum concentrations of leptin and insulin-similar growth factor I (IGF-I) may attune insulin resistance further, beyond the effects of adiposity and fat distribution [53]. Cross-sectional studies have shown that puberty is linked to a reduction in insulin sensitivity [54, 55]. In a serial study of 60 children spanning the pubertal transition from Tanner stages I to III, there was a reduction in insulin sensitivity by approximately i-third, and an increase in fasting blood glucose and insulin [56]. The autumn in insulin sensitivity was not associated with changes in body fat, visceral fat, IGF-I, androgens or oestradiol, and these changes were similar, regardless of sex, ethnicity or obesity.
Adiponectin is a novel adipocyte-derived peptide expressed predominantly in visceral adipose tissue [57, 58]. It is considered to have anti-diabetic, anti-inflammatory and anti-atherogenic effects, and has reduced levels in patients with coronary artery disease and diabetes mellitus in comparing with healthy people [57, 58]. Low plasma concentrations of adiponectin may be partly responsible for the atherogenic risk seen in patients with metabolic syndrome [57].
Resistin was discovered recently and is an adipocytokine expressed in homo, rat and mouse adipose tissue. The resistin gene is expressed almost exclusively in adipocytes [59], with increased expression in abdominal fat [threescore]. It has potential roles in regulating insulin resistance and adipocyte differentiation [59, 60], and may provide a possible link betwixt central obesity and type 2 diabetes mellitus and cardiovascular disease [60].
Body Limerick Is a Risk Factor for Developed Diseases
In that location are aspects of body composition that are risk factors for a multifariousness of common multi-factorial diseases in adulthood. The most apparent are those that issue straight from components of torso composition, namely obesity (TBF) and osteoporosis (BMC and bone mineral density) [four, 8]. As discussed above, these components tend to track over time. Adolescents who are overweight or obese during puberty are at greater risk of being overweight or obese every bit adults [37, 43], and those with depression BMC at peak bone mass are at greater risk of subsequent osteoporosis [four]. Similarly, lifetime overweight and obesity are major risk factors for cardiovascular affliction in adults [42, 61]. At that place are also strong relationships in children between trunk composition and run a risk factors for cardiovascular disease, such every bit blood pressure level. For instance, a divergence between the sexes in the relationship betwixt claret pressure and torso fat was observed in a written report of 920 African-American, Asian and Caucasian children anile five to eighteen years [62]. Using DXA and skinfold measurements, significant positive relationships betwixt systolic and diastolic blood pressure and trunk fatty, adjusted for TBF, were seen in boys at all pubertal stages in the three ethnic groups. In girls, all the same, torso fat was not a significant predictor of claret pressure.
Body Limerick during Puberty
A negative relationship between age at menarche, BMI and trunk fatness in girls has been shown [63, 64, 65]. It is still unclear, still, whether increased early childhood adiposity induces an earlier onset of puberty, if rapid maturation and early on puberty induce an increase in body fat subsequently in life, or whether both of these phenomena occur. In preliminary studies, nosotros examined growth, maturation and body composition using serial information from five,082 observations of a subset of 242 Causasian girls in the Fels Longitudinal Written report, who were built-in between 1929 and 1982 (i.east. girls for whom there were information until the minimum age of 21 years) [66]. Secular trends in body composition have emerged over the past few decades (e.yard. increases in adiposity), and then we hypothesized that insight into the relationships between serial indicators of maturation and body composition could be gained by examining data from children who were born at different times during the last century. The girls selected had an average of 21 serial observations each (range 6–44 observations). Age at menarche was collected prospectively at 6-month intervals.
Serial data on height, weight and BMI were analysed in two cohorts; Cohort 1 (built-in 1929–1954) and Accomplice 2 (born 1955–1982) were followed longitudinally from 6 years before menarche to half dozen years after menarche. For each girl, landmarks of growth in stature, including early childhood MHV, pre-pubertal MHV and boyish PHV, were determined using the triple logistic model of growth (fig. one) as implemented in the AUXAL software package [67]. The timings of several developmental landmarks from pre- to mail service-puberty in the two cohorts are shown in table 1. There were no significant differences between the 2 cohorts (i.e. no secular trend) in attaining these landmarks, including the age at menarche. Similarly, Chumlea and colleagues take concluded that there appears to be no secular trend in the historic period at menarche in girls in the U.s.a. over the past few decades [31].
Table 1
Longitudinal analyses were performed using mixed effects models, which considered an unstructured covariance construction, random effects (private) and fixed effects including intercept, slope (age), dispatch (age2), change in acceleration (age3), cohort, and cohort by age and cohort by agetwo interactions. As shown in table 2, there are no secular trends in stature during puberty; the 2 cohorts are virtually identical in terms of growth in stature [66]. There are, nonetheless, large and significant differences between the two cohorts in BMI at all fourth dimension points with the exception of the earliest time point, half dozen years before menarche (table ii). The BMI values across the 6 years before and afterward menarche in the 2 cohorts equally fitted from the longitudinal model are shown in effigy 2. Although it is not shown hither, a like difference betwixt cohorts is observed for BMI velocities (i.eastward. the charge per unit of change in BMI in individuals) [66]. Although BMI is not an ideal indicator of body composition in children, in the context of these analyses, the only plausible explanation for the large deviation in BMI between the cohorts and no difference in stature is that greater increases in adiposity occurred during puberty in Accomplice 2 compared with Accomplice 1.
Fig. ii
Table 2
If the main difference in body composition betwixt the two cohorts is the greater adiposity in Cohort 2, so tentative hypotheses most the human relationship betwixt adiposity and puberty tin be made by examining indicators of maturation in the two cohorts. In spite of significantly higher BMI levels in Cohort ii at various developmental landmarks, in that location are no differences between the cohorts in the timing of these landmarks [66]. Thus, to the extent that BMI is an indicator of secular increases in adiposity and considering the stability of indicators of growth patterns over time (eastward.thousand. the timing of physical growth landmarks and the age at menarche), the secular increase in BMI (adiposity) seen in the Fels Longitudinal Study from 1929 to 1982 did not have an effect on the rate of growth or sexual maturation in girls. Equally information from cohorts with more than contempo dates of nativity become bachelor, we tin examine this relationship and see how it relates to the electric current national surge in the prevalence of obesity.
Nosotros also performed other longitudinal analyses, using random effects models applied to serial data to characterize individual-to-private differences, allowing for fixed (same gradient) or random (differing slopes) furnishings of age and continuous indicators of maturation on various measures of torso limerick. We found that children in the Fels Longitudinal Written report who were more pubertally advanced than their peers, tended to exist taller and accept more TBF, BMC and FFM. Greater stature solitary could account for greater TBF, BMC and FFM, just per centum body fat, which is largely independent of stature, was higher in girls with an earlier historic period of menarche and onset of puberty (as measured using Tanner staging for breast development) than their afterward-maturing peers.
Conclusions
Throughout the recent history of evaluating torso composition and maturation during puberty, diverse methods of assessment have evolved. Techniques such every bit DXA and densitometry are better at analysing and quantifying TBF and FFM in children than BMI. A number of physiological changes occur during puberty, including rapid increases in physical size, hormonal fluctuations and marked changes in trunk composition, and the timing of various maturational landmarks during this catamenia is strongly related to concurrent body limerick. Furthermore, adipose tissue, as a major component of trunk composition, is involved in many hormonal interactions with growth and maturational factors during puberty that affect aspects of metabolic programming, including energy expenditure and insulin resistance. The majority of measures of body composition track from puberty into adulthood, and so cognition of the relative contributions of various body components (i.e. TBF, BMC and FFM) can atomic number 82 to a improve agreement of the natural progression of many chronic diseases including obesity, cardiovascular affliction, osteoporosis and diabetes. In addition, this knowledge allows predictions to be made well-nigh subsequent health outcomes and helps to place platonic timing for more effective primary illness prevention.
Acknowledgements
This work was supported by grants HD-12252, Hard disk-36342 and Hard disk-38356 from the National Institutes of Health, Bethesda, Maryland, USA.
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