Effects of Extracurricular Sports in Prepubertal and Pubertal Girls

: The aim of this study was to analyse the effects of the type of extracurricular sport on the body composition, respiratory parameters, and physical condition in prepubertal and pubertal girls. Four hundred and eighty-ﬁve female athletes (aged 8–14) from different sports participated in this study. They were gathered into four groups according to the sport typology and maturity level: ‘prepubertal girls who practise collective sports’ (PRE-CS), ‘prepubertal girls who practise individual sports’ (PRE-IS), ‘pubertal girls who practise collective sports’ (PUB-CS), and ‘pubertal girls who practise individual sports’ (PUB-IS). The cardiorespiratory ﬁtness (the 20 m shuttle run test, 20 mSRT), anthropometry, respiratory capacity (forced spirometry), handgrip, CMJ test, and stabilometry were collected. Prepubertal girls showed a lower muscle mass (kg) and fat mass (kg) than pubertal girls regardless of the extracurricular sports typology. PRE-CS and PRE-IS also showed a lower respiratory ﬁtness and physical ﬁtness than pubertal girls ( p < 0.05). Pubertal girls did not show signiﬁcant differences ( p > 0.05) in any of the body composition, respiratory ﬁtness, and physical ﬁtness variables when comparing between collective sports and individual sports. The results show that extracurricular participation in these types sports by prepubertal girls can inﬂuence their body composition, respiratory ﬁtness, and physical condition.


Introduction
Insufficient physical activity has a negative influence on the body composition, physical fitness, and health in children and adolescents [1,2]. This fact is worsened for those children by high levels of sedentary behaviour [3] or their suffering some health disease [4] because these have a detrimental effect on the development of sports skills [5]. These factors, together with the increasing sedentary time engaged in by children after school [6,7] might explain why paediatricians are reporting that today's youth is less strong, fast, and light than the previous generations [8].
This fact is substantiated by the increase in individuals with one, two, and even three syndromes of the 'paediatric inactivity triad' (PIT): 'paediatric dynapenia', 'exercise deficit disorder', and 'physical literacy' [8,9]. Thus, further effort in promoting physical activity is required [10,11]. Adolescence is probably the period in which higher morphological, physical, and physiological changes occur [12]. Many of these changes are influenced by lifestyle factors such as diet, unstructured physical activity, and organised sports participation [13,14]. Thus, it seems appropriate to control or monitor these parameters in prepubertal and pubertal adolescents. This is even more important for girls, because the changes in their body composition, physical, and physiological fitness occurring in adolescence play a significant role in the impact of the menopause later in the adulthood [15]. Furthermore, childhood and adolescence are key stages in the acquisition and establishment of healthy lifestyle habits [16].
One of the existing formulas to promote the physical activity and health of girls is extracurricular sport (organised sport practised by children and adolescents after school) [17]. In fact, around half of European children and adolescents take part in these activities [18]. However, girls still show less participation than boys [19].
Previous studies suggested that the typology of the practised sport can lead to a different body composition, along with physical and physiological adaptations in prepubertal and pubertal girls [20]. In addition, these two growth stages are key periods in the acquisition of morphological, physical, and physiological adaptations [21]. Nonetheless, there is limited information in this regard, as most studies are focused on the bone mineral mass and maturation [22,23] or do not compare different sports typologies [24]. Consequently, further research is required to understand the role of the typology of the extracurricular sport in the morphological, physical, and physiological adaptations of pubertal and prepubertal girls.
To provide an initial approach to this gap in the literature, this study aimed to analyse the influence of the extracurricular sport typology (individual and collective) on the body composition, respiratory parameters, and physical fitness of prepubertal and pubertal female girls. Furthermore, this work tested the hypothesis that extracurricular sports participation influences physiological adaptations in both prepubertal and pubertal girls. In addition, we expected that pubertal girls would show greater fat mass, respiratory parameters, and physical fitness than pre pubertal girls.

Design and Participants
This was a cross-sectional study. A total of 485 girls aged between 8 and 14 years enrolled in different extracurricular sports in Castilla-La Mancha (a region located in the centre of Spain) participated in the study. Participants took part in non-performance focused extracurricular sports for at least two days a week for at least one hour each day [25]. The study was conducted during the academic season. The final groups were 'prepubertal girls who practised collective sports' (PRE-CS; n = 111; 10.17 ± 1.58 years; 141.31 ± 0.12 cm; 39.66 ± 11.05 kg); 'prepubertal girls who practised individual sports' (PRE-IS; n = 230; 8.68 ± 2.05 years; 133.19 ± 0.14 cm; 32.84 ± 10.79 kg); 'pubertal girls who practised collective sports' (PUB-CS; n = 50; 13.90 ± 1.14 years; 157.08 ± 0.07 cm; 53.84 ± 10.72 kg); and 'pubertal girls who practised individual sports' (PUB-IS; n = 94; 13.87 ± 1.29 years; 159.85 ± 0.07 cm; 55.35 ± 10.72 kg).
Participants and their parents or legal guardians were informed of the study's objectives and the tests' characteristics. They signed the informed consent before starting the tests. The tests lasted between 60 and 90 min and were conducted in groups of 12 to 14 girls. The project was approved by the ethics committee of the university in which the study was conducted (Ref: 508; 17/04/2020).

Pubertal Status
Participants were individually evaluated to determine their pubertal status using the Marshall and Tanner test [26]. Stage I was categorised as prepubertal, while Stages II and III were classified as pubertal [27]. This test evaluates the development degree of girls' breasts and pubic villi in five different stages. It is a reliable and valid method used in many studies [27,28].

Anthropometric Measures Height
Height (cm) was measured using a SECA height metre (model 214; Hamburg, Germany), standing with the heels, glutes, back, and occipital region in contact with the height bar [27]. Girls were assessed with clothes and without shoes.

Body Composition
Weight (kg); body fat (%); body mass (kg) and skeletal muscle mass (%); fat mass in the upper body and lower body (%); and muscle mass in (kg) were measured by a portable segmental multifrequency body composition analyser (Tanita MC-780; Tanita Corporation, Tokyo, Japan). The body mass index (BMI) was calculated with the weight (kg) divided by the squared height of the girls [29]. Participants completed this test after an overnight fast without any intensive exercise on the day before [30]. For the tests, participants had to hold two handles with both hands during the impedance measurement (hand to foot BIA), performing a complete segmental analysis in less than 20 s [30].

Spirometry
Respiratory fitness was measured by forced spirometry (Portable Spirometer Spirobank II Advanced, France) [31]. Each girl performed a maximum inspiration after no more than two seconds of apnoea. Immediately afterwards they performed a maximum expiration until there was no air left in the lungs [31]. The forced vital capacity (FVC)-which is the volume delivered during an expiration made as forcefully and completely as possible, starting from a full inspiration-and the forced expiratory volume in one second (FEV)-which is the volume delivered in the first second of an FVC manoeuvre-were recorded [32]. The best result of two attempts was used for the analysis [29].

Manual Dynamometry
The upper-body muscular strength was assessed by handgrip strength with a hand dynamometer with an adjustable grip (TKK 5001 Grip A; Takei Scientific Instruments Co., Tokyo, Japan). The test was repeated twice with the dominant hand. The dominant hand was identified by asking the girls for the more comfortable hand to hold a racket [33]. To complete the test, girls had to close their dominant hand with their maximum force continuously for 2 s over the grip with their elbow position at its full extension [34,35]. The best score was taken for the analysis.
The results of the handgrip strength were expressed in kilograms (kg) and percentiles (pc) according to age [36,37].

Vertical Jump
The lower-body muscular strength was analysed using a countermovement jump test (CMJ) [34,38]. The jump height was calculated to the nearest 0.1 cm by two parallel photoelectric cells bars (Optojump, Microgate, Bolzano, Italy). These bars measured the time taken between the take-off and landing. The girls were instructed to jump as high as possible with a rapid, preparatory downward eccentric action, while their arms were able to be moved freely [38]. The best of three attempts (with 1 min. of recovery between trial) was selected for the analysis. The results of the CMJ were also standardised using the values of percentiles (pc) according to age [36,37].

Stabilometry
The distribution of pressure of the participants when standing on two legs was recorded by a portable baropodometry platform (Footwork ® platform AM3-IST ® ; Paris, France). The test consisted of the participants standing upright and barefoot on the centre of the platform for 30 s while looking at a fixed point with their hands on their hips [39].
The results were expressed in percentage units (percentage of the difference between right and left leg).

Physical Condition: Course Navette Test
The Course Navette test (20 m shuttle run test (20 mSRT)) was used for assessing the cardiorespiratory fitness [40]. The test finished when the girls failed to run the full length of the 20 m line according to the audio signal beep two times in a row or if stopped because of fatigue. The results of the test were standardised using the values of percentiles (pc) and percentiles according to age [36,37]. The 20 mSRT was the final test conducted in the protocol, so that fatigue did not interfere with the previous tests [34].

Statistical Analysis
Data are presented as means ± standard deviations. The normality of the variables was confirmed by the Kolmogorov-Smirnov test. A two-way analysis of variance (two-way ANOVA) was used to analyse the differences in body composition, physical condition, and cardiorespiratory variables according to the type of sport (collective or individual) and the pubertal status (prepubertal or pubertal). Pairwise comparisons were carried out by the Bonferroni post hoc test. Furthermore, in addition, the confidence interval (CI of 95%) was calculated to identify the magnitude of the changes and effect sizes (Cohen's d, ES) were calculated and defined as follows: trivial, <0.19; small, 0.2-0.49; medium, 0.5-0.79; large, >0.8 [41]. The level of significance was set at p < 0.05.

Results
The outcomes regarding the body composition are displayed in Table 1. Prepubertal girls showed a lower BMI (p < 0.05; ES = 0.66-1.02), fat mass (in both percentage (p < 0.05; ES = 0.28%-0.62%) and kilograms (p < 0.05; ES = 0.91-1.37 kg)) and muscle mass (in kilograms; p < 0.05; ES = 1.75-2.16 kg) values than pubertal girls regardless of the sports typology. Prepubertal girls also revealed a lower muscle mass in kilograms (p < 0.05) in their body trunk, both of their arms, and both of their legs than pubertal girls regardless of the sport typology. Finally, PRE-ISs showed a higher muscle mass (in percentage) than PUB-ISs and lower fat mass (in percentage) than PUB-ISs in their body trunks, both of their arms, and both of their legs (p < 0.05). PRE-CSs also displayed a lower fat mass (in percentage) in these three body segments than PUB-CSs, but significant differences were found only for the right leg (p < 0.05). The comparisons between collective and individual sports revealed PRE-CSs to have a significantly higher BMI (+1.21%; p < 0.05; ES = 0.36; 95% CI: 0.41%-2.01%), fat mass (in percentage (p < 0.05; ES = 0.26; CI: 0.16%-2.74%) and kilograms (p < 0.05; ES = 0.49; CI: 1.16-3.56 kg)), muscle mass (in kilograms; p < 0.05; ES = 0.65; CI: 2.83-5.62 kg), and muscle mass in the three body sections (trunk, arms, and legs; p < 0.05) than PRE-ISs. On the contrary, PUB-CSs did not show significant differences in their body composition in comparison to PUB-ISs, except in the percentage of fat mass in their right legs (−1.86%; p < 0.05; ES = 0,30; CI: between −0.05% and −3.76%).
The results of the respiratory variables are presented in Table 2. Prepubertal girls displayed significant lower values than pubertal girls in all respiratory variables (p < 0.05; ES = 1.23-2.31) except FEV 1 _FVC (p > 0.05) regardless the sport typology. The comparisons between sport typologies revealed that PRE-CSs had higher outcomes than PRE-ISs for FVC, FEV 1 , PEF, and FEF 2575 (p < 0.05; ES = 0.61-0.71) but not for FEV 1 _FVC (−0.12%; p > 0.05; ES = 0.02; CI: between −1.60 and 1.34). On the contrary, PUB-CSs and PUB-ISs did not show significant differences in any of the studied variables.    , mean forced expiratory flow between 25% and 75% of FVC l ; L, litres; L/s, litres per second. * Difference in respiratory variables between prepubertal and pubertal girls for each sports typology, p < 0.05. † Difference in respiratory variables between individual or collective sport for each pubertal stage in girls, p < 0.05.
The outcomes of the physical tests are displayed in Table 3. Prepubertal girls showed a lower handgrip (kg), Course Navette test score (stages), and vertical jump (cm) performance than pubertal girls (p < 0.05; ES = 0.80-2.04) regardless of the sport typology. Furthermore, PRE-ISs also showed significantly higher values for the Course Navette

Discussion
This is the first study that analyses the influence of the extracurricular sport typology on the body composition, respiratory fitness, and physical condition of prepubertal and pubertal girls. The main findings were that morphological, physical, and respiratory adaptations vary according to the growth stage (i.e., prepubertal and pubertal) and the practised extracurricular sport (i.e., individual or collective). However, significant differences according to the extracurricular practised sport were found only in prepubertal girls, partially confirming the initial hypothesis.
The existing evidence suggests that the transition from prepuberty to puberty increase girls' fat mass regardless of their daily physical activity [42]. This study is line with this evidence and our second hypothesis, as pubertal girls (either PUB-CSs or PUB-ISs) showed higher fat mass pubertal girls. However, this is a cross-sectional study, while diet and active life were not controlled, so cause-effect cannot be set from this study. The transition from prepuberty to puberty is also associated with a muscle mass increase in girls [43,44]. Nonetheless, this increment seems to be higher in girls participating in extracurricular sports [19,45]. This might explain why both pubertal groups showed a higher muscle mass even when the average age (PUB-CS = 13.90 ± 1.14 years; PUB-IS = 13.87 ± 1.29) was lower than the age period (around 15 years old) during which muscular strength and muscle mass gain are accelerated [43]. The fact that both fat mass and muscle mass increase during adolescence also explains why both groups (PUB-CS and PUB-IS) displayed higher BMI levels than the prepubertal girls, which is in line with a previous study in pubertal girls participating in extracurricular sports [46]. Thus, care must be taken when tracking changes in adolescence using the BMI.
It has been suggested that the extracurricular sport typology plays a significant role in the body composition [47]. However, this is partially evidenced in the current study as PUB-CSs and PUB-ISs did not show differences in their body composition. It is important to highlight that only two sport typologies were defined in this study, so future studies attempting to confirm or reject our findings should consider more sports typologies. The fact that PRE-CSs showed a higher muscle mass might be due to the demands of collective sports (i.e., jumps, changes of direction, acceleration, deceleration, sprinting, etc.) [48]. However, additional studies are needed to confirm these findings. Furthermore, PRE-CSs showed a higher fat mass and percentage fat mass than PRE-ISs, which might be due to the demands of the practised sports but also due to their food habits [49] or daily activity. Therefore, future studies should also attempt to control the diet of prepubertal and pubertal girls and measure the daily activity.
In line with previous studies [50], girls' pulmonary capacity improved with age regardless of the sport typology. This might be due to several reasons; however, maturity is likely to be the main reason for the higher respiratory capacity of pubertal girls, as it causes an increase in the lungs' dimensions and the muscles participating in breathing [51,52].
Exercise has been associated with a higher respiratory capacity in both prepubertal and pubertal girls [53]. However, most of the studies analysing lung capacity in these populations have focused on one sport, with swimming being the most common one [54]. Thus, the role of the extracurricular sport typology in the pulmonary adaptations before and after the menarche in girls remains unknown. Our findings suggest that the exercise typology might cause different respiratory fitness adaptations in prepubertal girls, but this was not evidenced in pubertal girls, partially confirming the first hypothesis. Although cause and effect cannot be established, one of the reasons for PRE-CSs having greater respiratory adaptation might be the intensity of the exercise performed [55], which might somehow be reduced in PRE-ISs in order to get an accurate sports technique. Subdividing individual and collective sports into further categories, as well as monitoring the training load (e.g., through heart rate), might provide additional information about the role of extracurricular sports on the pulmonary capacity of both prepubertal and pubertal girls.
Regarding the physical fitness parameters, PRE-IS and PRE-CS girls showed a lower handgrip, and Course Navette and vertical jump performance than PUB-IS and PUB-CS girls. This was expected, as maturity improves the physical fitness and strength [43,55]. When comparing the two selected extracurricular sports typologies, PRE-ISs showed a lower handgrip, handgrip percentile, and Course Navette score (stages) than PRE-CSs. This was probably due to the demands of the practised sports, as the intensive training stimulus of collective sports improves the maximum aerobic power and strength of prepubescent children [56]. The fact that PRE-ISs showed a higher vertical jump percentile than PRE-CSs might somehow contradict our previous statement; however, it has been reported that strength and coordination play a key role in prepubertal children's jumping ability [57,58], so that might be the reason why PRE-ISs achieved a higher percentile in the CMJ test [59]. On the other hand, no significant differences between PUB-CSs and PUB-ISs were found for physical fitness. Once again, it is likely that the absence of significant differences was due to only two sport typologies being identified. Therefore, further studies are required to understand the role of sport typology in the physical parameters of pubertal girls. This is an initial attempt to address a gap identified in the literature, and therefore the reason why only two sport typologies were defined. Another significant limitation is that this is a cross-sectional study, in which factors such as diet or life activity were not controlled, so cause and effect cannot be established. Future studies should attempt to overcome these limitations by comparing more categories of both individual sports and collective sports and controlling girls' dietary habits and life activity. The measurement of the body composition was measured by a Tanita, which is less accurate than the gold standard (Hologic Series Discovery QDR, Software Physician Viewer, APEX System Software v 3.1.2; Bedford, MA, USA) [27]. However, the Tanita has proven to be effective in comparing a large number of population groups [60,61]. The physical condition was also measured indirectly, but again, this formula is suitable for measuring and comparing large population groups [62].

Conclusions
Extracurricular sports (of individual and collective modality) are not a determining factor on the physiological parameters of pubertal girls, but they cause different physiological adaptations in prepubertal girls. Pubertal girls participating in extracurricular sports have a greater fat mass percentage, respiratory capacity, and physical fitness than prepubertal girls. Institutional Review Board Statement: The project was approved by the ethics committee of the university in which the study was conducted.

Informed Consent Statement:
The participants signed the informed consent before taking part in the study.

Data Availability Statement:
The datasets generated and/or analysed during the current study are not publicly available, because when we conducted the study, we specifically committed to both participants and extracurricular activity provider chains that the collected data were not going to be shared with third parties or people. However, they might be available from the corresponding author on reasonable request.

Conflicts of Interest:
The authors declare that they have no competing interests. This study was carried out in accordance with the recommendations of the Declaration of Helsinki with written informed consent obtained from all subjects. The project was approved by the Bioethics Committee for Clinical Research of the Virgen de la Salud Hospital in Toledo (ref.: 508/17042020).