1. Introduction
Biological maturation is a natural lifelong process that promotes morphophysiological changes in individuals [
1]. Biological age is, therefore, defined by the individual maturation rhythm of each person. Thus, biological maturation depends on genetic, nutritional, and environmental factors; thus, the improvement of neurological, endocrine, bone and muscular systems that occur throughout life [
1,
2]. During this process, puberty is a milestone due to the occurrence of faster maturity, mediated by the increase of estrogen group steroid hormones [
3,
4,
5,
6]. This group of hormones play an important role in female biological characteristics and may influence the onset of menstrual period and the development of secondary sexual characteristics [
7,
8,
9].
Typically, growth hormones reach a peak during the pubertal process [
1,
2,
10,
11]. In females, the growth hormone peak activates the hypothalamic–pituitary–ovary axis, promoting the production of estrogens (estradiol, estrone, estriol, and androstenedione) [
1,
4,
12,
13]. It is worth mentioning that among the estrogens produced by the female organism, this organism stands out for having an intense link with the reproductive function, and it is during the puberty phase that, among the functions in the organism, its production is accentuated. This is in addition to providing stimulation of the release of eggs by the ovarian follicles and acting on the fallopian tubes (i.e., female organ) by stimulating muscle contractions in the endometrium, raising its levels in the female menstrual phase [
3,
4,
5,
7].
Previous studies have demonstrated a relationship of maturation with neuromotor performance, exposing that biological maturation can influence the vertical jump skills, countermovement jump, strength of the upper limbs, in the neuromotor control of the muscles involved in the trunk region [
14,
15,
16,
17]. Furthermore, within sports, maturation can influence the quality of execution of specific skills (i.e., performance in Olympic rowing, basketball and volleyball, among others) [
14,
15,
16,
17,
18,
19]. Besides that, an increase in estradiol concentrations throughout the maturation process and the accurate development of the neuromotor system. In other words, the interaction between nerve impulses and the skeletal muscles that generate movement increases, leading to maximal voluntary strength of the biceps brachii and knee extension [
20,
21].
In addition, a linear association between sex hormone levels and strength development has been suggested. The association can be explained by the interaction of sex hormones with protein synthesis, which results in an increase in the lean mass and contributes to gain in muscle strength [
22,
23,
24]. Additionally, due to the abundance of hormones at puberty, especially in female participants [
4], intramuscular hormone receptors for estrogen hormones such as estradiol, for example, frequently act in the regulation of metabolism [
25].
Moreover, the metabolism ends up being stimulated by several mechanisms such as muscle contraction generated by neuromotor activities that require more recruitment of type II muscle fibers (i.e., fast-twitch muscle fibers stimulated by the anaerobic energy pathway; and muscle fibers stimulated predominantly in muscle power activities). In this context of biological systems altered by maturation, the skeletal muscle process tends to gain prominence due to constant changes due to the human growth process [
26].
In this sense, it is likely that one of the mechanisms related to strength gain during the maturational process is hormone-mediated [
25,
26,
27]. Thus, in view of the foregoing, our hypothesis is that the maturational stages and levels of hormone markers in the body may be significantly related to the performance of neuromotor skills. Therefore, the objective of the present study was to verify the relationship between hormonal markers and biological maturation markers on the neuromotor capacities of young females.
3. Results
Table 1 reports the characterization of the sample. Describing in a descriptive way that the evaluated participants presented bone age similar to chronological age, a peak of growth speed with classification during peak of growth and estradiol levels more abundant than the levels of testosterone.
Table 2 presents the correlation matrix between hormones and maturation and strength performance. Estradiol is related to the maturation process of girls, as well as power performance. On the other hand, testosterone was not related to the peak growth rate, but was related to power capacity. In relation to the variables of upper limb velocity and body velocity with change of direction, there were no significant correlations. The analyses controlling the effect of the maturation variables on the relationship with the hormonal markers did not show statistical significance. In relation to somatic maturation, 17 subjects were classified into pre-peak growth velocity, 22 during-peak growth velocity and 5 post-peak growth velocity.
Figure 1 shows the hormonal levels according to the maturation stage and it was evident that estradiol levels tend to increase significantly with advancing biological maturation (F
(41,0) = 8.13;
p = 0.001), whereas for Testosterone concentrations did not show significant differences between maturational stages (F
(41,0) = 0.75;
p = 0.4).
Table 3 presents the correlation matrix between maturation and strength performance. Peak speed growth is related to lower and upper limb power production capacity. The same was true for bone age. No relationship was found between maturation and the variables of upper limb velocity and body velocity with change of direction. When controlling the effect of hormonal markers on the relationship of neuromotor variables with those of maturation, it was found correlation for the power of upper and lower limbs remained statistically significant.
The regression models of maturational and neuromotor variables along with estradiol and testosterone levels are detailed in
Table 4. The peak of the speed of growth, bone age, and neuromotor performance of lower limbs were found to be statistically significant.
The regression models of hormonal and neuromotor variables with skeletal and somatic maturation are shown in
Table 5, so the analyses were statistically significant for estradiol levels, and for lower and upper limb potency.
Table 6 reports that the perceptron artificial neural networks concluded with the results that skeletal maturation (bone age) has more than 50% probability of being able to predict the strength of the upper and lower limbs, and the somatic maturation (peak of the speed of growth) indicates a potential of more than 60% to anticipate the performance of upper and lower limbs, the speed of upper limbs, and the change of body direction at high speed. Yet, hormonal markers indicate a more than 95% chance of foreshadowing the strength of upper limbs.
4. Discussion
The aim of the present study was to verify the relationship between hormonal markers and biological maturation markers in the neuromotor abilities of female children. Similar to the objective of the present study, Lowe et al., [
37] addressed that hormonal markers in the group of estrogens including estradiol interact with strength levels in women throughout life, and Aslam et al., [
8] recently reported that there is a relationship between hormone levels during puberty and neuromotor skills in subjects of both sexes. In the same context to the objective of the present study, seeking to find relationships between maturation and neuromotor performance, Volver et al., [
27], in a longitudinal study, analyzed 34 female subjects aged between 11 and 13 years old and, the authors concluded that sexual maturation influences neuromotor skills suggesting a possible interaction of factors related to puberty, such as hormone levels for example.
Thus, the results of the present study corroborate with the aforementioned studies and also with the statements of Sadiq et al., [
10], where the authors highlighted that biological maturation is available for hormonal markers and that they can be used with different methods of the human body, cardiovascular, neurological and musculoskeletal system.
In this sense our data suggest that maturation is related to sex hormones, but in girls testosterone is not a major factor in peak growth velocity (
Figure 1) and that both maturation and hormones are related to strength development in girls; however, they were not related to upper limb velocity and body velocity with change of direction (
Table 2 and
Table 3). The maturational process develops endocrine tissues to the point where their hormonal production capacity is high, near the growth spurt [
4]. Moreover, the development of the hypothalamus-pituitary-gonads and hypothalamus–pituitary–adrenal axis act on the development of sexual characteristics (i.e., sexual maturation) [
1] and changes in body composition [
38]. However, as shown in
Figure 1 of the results of the present study, this relationship between hormones and maturation should not be analyzed solely by chronological age, since there may be differences in hormonal responses in children of the same age due to distinct maturational stages [
22].
Moreover, a relationship between hormone concentrations (
Table 2) and biological maturation assessed by different methods (
Table 3) and the level of muscle strength was demonstrated. In fact, maturation induces changes in neuromotor behavior in young people, mainly related to force [
39]. In addition to hormonal changes, changes in muscle composition, energy metabolism, and neural develop during maturation and together develop the ability to produce strength [
23].
Given this assumption, our findings indicate that with the advancing maturation, the levels of estradiol (female sex hormone) tend to increase (
Figure 1). Our findings differ with the study by Pinto et al. [
40], where the authors evaluated 89 children of both sexes aged between 10 and 13 years. The data from that study pointed out that for male and female participants, there were no statistical differences in relation to hormone levels with advancing sexual maturation stages. However, it was observed that in neuromotor skills there were no significant differences between the maturation stages of males, while in females, maturation stages III and IV (advanced) were superior to I and II (delayed) in relation to muscle power of the upper limbs.
It is noteworthy that in our results the neuromotor capacities showed correlations with the maturation evaluated by different protocols both for the power of upper limbs (bone age: r = 0.55;
p < 0.0001; Peak growth velocity: r = 0.59;
p < 0.0001) as for the power of lower limbs (bone age: r = 0.58;
p < 0.0001; Peak growth velocity: r = 0.57;
p < 0.0001). In this way, the power of upper limbs corroborated with the results found by Pinto et al. [
22], where the authors found significant correlations of maturation with the muscular power of upper limbs but found no significant data for lower limbs potency. Júnior et al. [
41] in their study also evaluated the power of lower limbs in a sample consisting of 46 school athletes of both sexes (aged 12 ± 3 years), and did not find results with significant values (
p = 0.08), diverging from our findings.
In regard to the correlation between bone age and estradiol, our data (bone age x estradiol: r = 0.58;
p = 0.007) were positive corroborating with those of Pinto et al., [
22] where a strong correlation of estradiol with bone age (r = 0.51;
p = 0.001) was exposed. Therefore, it is noteworthy that in relation to testosterone our findings evidenced that the bone age also had a strong correlation (r = 0.51;
p = 0.005), and this can be justified by the statements of Forrest [
42] and Wirth et al., [
43], the authors discuss that the testosterone has participation in bone development, influencing osteogenesis in particular during growth.
In relation to the hormonal levels, the muscular power of the lower limbs (estradiol: r = 0.52;
p = 0.007; testosterone: r = 0.42;
p = 0.03) and higher (estradiol: r = 0.52;
p = 0.006; testosterone: r = 0.42;
p = 0.02) in our data were presented relations for estradiol levels; and for testosterone levels, in relation to estradiol the results found by the present study diverge from the results of Pinto et al., [
22], where in relation to estradiol the correlation was not significant for the muscular power of limbs inferior (r = 0.15;
p = 0.3) and it was significant for upper limb power (r = 0.37;
p = 0.01).
The regression models of the study (
Table 4 and
Table 5) indicated that estradiol levels could assist in predicting peak growth speed, bone age, and lower limb neuromotor performance in the study participants. However, caution should be exercised in interpreting the values because regression determination coefficients revealed trivial magnitudes. In this study, testosterone levels did not indicate significant results in relation to the statistical regression models. However, analyses of artificial neural networks (
Table 6) indicate that maturation can predict neuromotor performance by more than 50% and that hormonal markers have a potential of more than 95% for the probability of correct answers in relation to the prediction of upper limb performance.
In view of this approach, it is worth mentioning that hormonal levels influence the acquisition of lean mass and that lean mass is closely linked to the production of strength during the execution of neuromotor skills [
4,
23,
27,
44,
45], and in this context young people with biological maturity accelerated body weight, greater concentration of lean mass, and a higher concentration of hormone levels [
1,
22,
23,
46]. This fact can also be confirmed in the results of the present study, corroborating the findings of Goswami et al. [
26], where the authors showed that the muscular power of the lower and upper limbs is associated with maturation and that this association is significantly influenced by sex hormones, and that discriminating that with advancing maturation stages, the concentrations of hormone levels tends to increase.
In this sense, given that muscle strength is associated with the performance of various sports [
44], autonomy from daily living activities, biomechanical functionality and that higher levels of strength are related to decreased risk of cardiovascular disease [
47]. The findings of the present study are important to widen knowledge on how muscle strength is built until adulthood, explaining the importance of awareness of the maturation stage in young people. Considering that hormone levels can interact with the acquisition of lean mass and neuromotor performance, it is necessary to understand that individuals with similar chronological ages can have different levels of maturation and this can directly interfere with hormone levels (
Figure 1).
Therefore, the future perspectives are that health and sport professionals have a particular perspective at the maturation process, using the findings discussed in this research in their professional practice. Thus, a possible practical applicability aimed at health professionals is the monitoring of maturation stages during interventions involving hormonal therapies (for young people who have growth deficit, or have a muscle strength profile below that expected that interferes with daily functionality). Sports professionals can use maturation assessment to monitor strength levels and associate them with the possible stage of neuromotor development that the participants find themselves in a non-invasive manner and with a low financial cost.
However, despite the relevance of the results, the present study has some limitations: Firstly, the fact that the study design is observational, which does not allow establishing a cause and effect relationship. Secondly, it was not possible to perform a longitudinal follow-up during the puberty period of the analyzed participants. Thirdly, the sample was made up only of female participants. Therefore, it is important to carry out new studies where there may be a longitudinal assessment and in both sexes.