Early Human Development 91 (2015) 327–331
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Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Digit ratio (2D:4D) and physical fitness (Eurofit test battery) in school children R. Ranson a, G. Stratton b,c, S.R. Taylor a,⁎ a b c
Sport & Exercise Sciences, Glyndwr University, Wrexham LL11 2AW, UK Applied Sports Technology Exercise and Medicine Centre (A-STEM), Swansea University, Swansea, UK School of Sport Exercise and Health Sciences, University of Western Australia, Crawley, WA 6160, Australia
a r t i c l e
i n f o
Article history: Received 30 November 2014 Received in revised form 23 February 2015 Accepted 16 March 2015 Keywords: 2D:4D Eurofit Children's fitness Testosterone Anthropometrics
a b s t r a c t Background: The relative lengths of the index finger to the ring finger (2D:4D) is sexually dimorphic and is thought to be a correlate of prenatal sex steroids (low 2D:4D = high prenatal testosterone and low prenatal oestrogen). In adults there have been reports that low 2D:4D is consistently associated with high sports performance. Aims: To investigate correlations between 2D:4D and fitness levels in children. Study design: Right 2D:4D and body size were measured, in addition to flexibility, speed, endurance and strength (Eurofit tests). Subjects: 922 boys and 835 girls (mean ages (years): 10.8 ± 1.01 and 10.07 ± 1.00 respectively). Outcome measures: height, mass, BMI, triceps and subscapular skinfolds, 20 m shuttle run, sit and reach, standing broad jump, hand grip strength, 10 × 5 m sprint, and the sit and reach test. Results: Boys significantly outperformed the girls in the 10 × 5 m sprints, the 20 m shuttle run, standing broad jump, and hand grip strength. In boys but not girls, 2D:4D was significantly negatively correlated with scores in all these tests except the standing broad jump. In girls but not boys, 2D:4D was significantly positively correlated to stature, mass, BMI and waist circumference. Conclusions: It is suggested that high prenatal testosterone and low prenatal oestrogen (low 2D:4D) is implicated in high sprinting speed, endurance and hand grip strength in boys. In girls low prenatal testosterone and high prenatal oestrogen is associated with large body size. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction The multifactorial nature of the male advantage in sport, and the sex differences in physique, are thought to be partly a result of prenatal effects of testosterone on the brain and/or on the cardiovascular system [1,2]. One correlate of prenatal testosterone is the relative lengths of the 2nd (index finger) and 4th (ring finger) digits (2D:4D) and the 2D:4D ratio is negatively related with prenatal testosterone and positively with prenatal oestrogen [3–5]. Many studies have shown that males generally have relatively shorter 2nd digits than 4th digits compared to females [6,7] which results in a lower, “more masculine” 2D:4D associated with higher prenatal testosterone levels [8]. The relative sizes of the fingers are established in utero and the ratio is reported to be stable during postnatal growth and throughout puberty [9,3]. Therefore, if 2D:4D remains relatively constant during life, and there is a relationship between 2D:4D and fitness or sporting ability, then the ratio may be useful as a talent identification tool [1,10]. The benefits of regular participation in physical activity throughout childhood are well documented [11]. However in recent years there ⁎ Corresponding author at: Glyndŵr University, Wrexham Campus, Mold Road, Wrexham LL11 2AW, UK. Tel.: +44 1978 293092. E-mail address: [email protected] (S.R. Taylor).
http://dx.doi.org/10.1016/j.earlhumdev.2015.03.005 0378-3782/© 2015 Elsevier Ireland Ltd. All rights reserved.
has been an increase in sedentary behaviour and a significant decline in aerobic fitness (average decline of 0.43% per year) in the child population [12]. Data from the UK show that aerobic fitness has declined at a rate of 1.3% and 2.3% per year in boys and girls respectively from 1998 to 2010 [13]. The Eurofit tests assess various principle components of physical fitness, both health- and skill-related fitness characteristics [14]. The Eurofit tests have been widely used due to their simple administration [15] and normative data that can detect status changes and trends. There are a number of studies into the relationship between 2D:4D and sport performance, although results have often been based on small sample sizes and have been performed on adult males [10]. A lower 2D:4D has been reported to be related to high achievements in the following: men's professional football, [1] and in a range of men's sports, [1] female athletic ability, [16] endurance running times for men and women [17], slalom skiing times for men and women [18], and rowing times for women [19] . A major limitation of 2D:4D and sporting ability studies in the literature, is that the evidence is often based on selection and rankings which are prone to several sources of bias such as selection effects based on game intelligence, resilience as well as subjective ‘views’ from coaches [10,17]. Research on the relationship between children's 2D:4D and health and fitness is limited. Of the available literature
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Hönekopp et al. [2] examined the relationship between 2D:4D and physical education (PE) grade in teenagers. The PE grade however reflects attainment levels in a variety of physical activities and not a specific measure of fitness. The attainment levels are therefore based on subjective rather than objective measures. In one of the only studies to objectively assess performance measures, Peeters et al. [20] examined the relationship between 2D:4D and health- and skill-related fitness in Flemish children and showed no relationship between digit ratio and various components of physical fitness. However, the study was limited to girls, who were aged 6–18 years and based on left hand 2D:4D and therefore has limited application, ideally the study should be repeated using the right or both hands [20]. To our knowledge there are no studies that have examined the relationship between 2D:4D and fitness in both boys and girls. If fitness is related to the effects of prenatal sex steroids we would expect that 2D:4D will be correlated with fitness in pre-pubertal children. Therefore, the purpose of this study was to examine the relationship between 2D:4D and healthand skill-related fitness tests in school children. It was predicted that children with a low 2D:4D would perform better in the Eurofit tests than children with high 2D:4D. 2. Methods 2.1. Participants and procedures The university Research Ethics Committee approved the study which involved 1776 Welsh school children recruited from primary and secondary schools aged 8–12 years (boys 10.1 ± 1.0 years; girls 10.1 ± 0.9 years). Almost all of the participants were Caucasian children (97%), with a few East Asian and Black children. Inclusion of all ethnicities made little difference to subsequent analyses. Therefore, we report results from the complete sample. Every school, parent/ guardian and pupil gave informed consent and assent respectively and had the right to withdraw. All fitness testing was performed on the same day of the week between 09:00 and 15:00 h. Participants undertook a standardised 10-minute warm up consisting of dynamic stretches to music. Right hand 2D:4D was measured using a digital camera (Sony Cyber-shot, Singapore) and Adobe Photoshop software (Adobe systems, San Jose, CA) following the procedures outlined by Ranson et al. [21]. All the photographs were coded to ensure that the researcher measuring digit length was blinded to the fitness scores and the appearance of the individual child to reduce experimenter bias [22]. BMI was calculated as body mass in kilogrammes divided by the square of stature in metres (kg/m2). Triceps and subscapular skinfolds were measured using Harpenden callipers (John Bull British Indicators, West Sussex, UK) to the nearest millimetre and per cent body fat (%BF) was calculated using the methods outlined by Lohman [23]. All children participated in the 20 m shuttle run (20MSFT) to measure aerobic fitness [24], sit and reach (SR) to quantify the level of flexibility, standing broad jump (SBJ), to examine leg power, hand grip strength (HG) to measure strength and the 10 × 5 m sprint (10 × 5 m) tests to test sprint performance [14]. An additional test was also administered; the modified sit and reach test (mod SR) was used to assess flexibility whilst taking into account limb length [25]. Participants were given a demonstration and a practice attempt before performing each test, and were encouraged throughout. The highest score was recorded for HG, SR, mod SR, and SBJ where the children had 3 attempts. All tests were administered by a trained member of the research team. 2.2. Statistical Analysis Descriptive statistics were calculated using Microsoft Excel (2007) and the statistical analyses were performed using IBM SPSS (v.19) software. Normality of the data was checked and Pearson's correlation and standardised linear regression coefficients were used to investigate
relationships between 2D:4D and the health and fitness scores. All data were tested for normality using Kolmogorov–Smirnov as the data set included more than 50 participants [26]. The data were corrected for age and BMI to normalise the data for the morphological changes that occur during adolescence. An alpha level of p ≤ 0.05 was used as the criterion to determine significance. 3. Results There were 1776 participants in the sample. However, not all participants were measured for all variables. Therefore, numbers per variable differed somewhat. Means (± SD) for age, stature and mass were as follows: boys, age n = 911, 10.08 ± 1.01 years; stature n = 917, 141.7 ± 8.51 cm; body mass n = 917, 37.1 ± 9.27 kg; girls age n = 814, 10.07 ± 1.00 years; stature, n = 827, 141.2 ± 9.59 cm; body mass n = 823, 37.4 ± 10.48 kg. 3.1. Repeatability of 2D:4D The lengths of the 2nd and 4th digits of the right hand were measured on two separate occasions, with the second measurements performed by the same measurer and blind to the first measurements in 50 participants (boys n = 25; girls n = 25). From these two sets of measurements 2D:4Da and 2D:4Db were calculated. The Pearson's correlation coefficients of 2D:4Da compared to 2D:4Db was high (r = 0.95), as was the intra-class correlation (r = 0.90), whereas the coefficient of variation (CV) was very low (0.9%) [21]. Therefore, we concluded that our measurements of 2D:4D reflected real betweenindividual differences. 3.2. Sex differences Boys had a significantly lower mean 2D:4D (n = 922, 0.939 ± 0.034) than girls (n = 834, 0.952 ± 0.034; t = 8.07, p b 0.0001). The digital ratio data were found to be normally distributed (Z = 0.019; p = 0.146) but age and BMI were found to deviate from the normal distribution (p b 0.05), however the data were included in the linear regression as it has been suggested that in large samples this is not a requirement [27]. We found significant sexual dimorphism in the performance variables (Table 1). Boys had higher scores in the MSFT, ran faster 1 / 10 × 5 m, jumped further in SBJ, and were stronger for HG. In the SR and the mod SR girls were more flexible than boys. With regard to body size and composition (Table 2) we found significant sexual dimorphism in % body fat and leg length such that in comparison to girls boys had lower % body fat and longer legs. 3.3. 2D:4D and performance Digit ratio was sexually dimorphic. In addition, we found that 2D:4D was weakly but significantly related to age (n = 1725, r = 0.05, p = 0.04) and BMI (n = 1741, r = 0.06, p = 0.02). Therefore, we performed
Table 1 The means (±SD) for sex differences in the performance variables. There is a significant male advantage in MSFT, 1 / 10 × 5 m, SBJ, HG, and PT and a significant female advantage in SR and mod SR. Note that, in order to reverse the sign of the results for 10 × 5 m we transformed the times (1 / 10 × 5 m). Test
Boys (n)
Boys Mean ± SD
Girls (n)
Girls Mean ± SD
t
p
MSFT 1 / 10 × 5 m SBJ HG SR Mod SR
872 899 912 916 915 913
39.06 ± 17.43 0.044 ± 0.004 138.92 ± 21.06 16.94 ± 4.47 14.22 ± 6.3 24.54 ± 5.62
782 815 832 831 828 830
28.96 ± 12.73 0.042 ± 0.004 128.97 ± 19.29 15.65 ± 4.27 19.16 ± 6.62 28.57 ± 6.29
13.33 10.67 10.26 6.15 15.96 14.10
0.0001 0.0001 0.0001 0.0001 0.0001 0.0001
R. Ranson et al. / Early Human Development 91 (2015) 327–331
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Table 2 The means (±SD) for sex differences in body size and body composition variables. Males had significantly lower % fat and longer legs than females. Trait
Boys (n)
Boys Mean ± SD
Girls (n)
Girls Mean ± SD
t
p
% fat Leg length Stature Mass BMI Waist
913 855 917 917 917 912
21.09 ± 8.63 70.50 ± 5.80 141.72 ± 8.51 37.13 ± 9.27 18.28 ± 3.13 62.79 ± 8.51
821 776 827 823 823 825
27.51 ± 6.74 69.55 ± 6.26 141.22 ± 9.59 37.46 ± 10.48 18.52 ± 3.48 62.48 ± 9.74
17.12 3.19 1.15 0.69 1.50 0.72
0.0001 0.002 0.25 0.49 0.14 0.47
a number of multiple regressions and considered the relationships between 2D:4D and performance in boys and girls separately, removing the influence of age and BMI (Table 3). Note that, in these regression analyses the independent variables were forced simultaneously into the analysis. This minimised the possibility of multicollinearity. For comparison purposes we changed the direction of the performance variable 10 × 5 m by transforming it to 1 /10 × 5 m. We found negative relationships between 2D:4D and four performance variables in boys. That is, in comparison to high 2D:4D boys, low 2D:4D boys ran faster in the 10 × 5 m (1 / 10 × 5 m: Fig. 1), completed more runs in the MSFT and had stronger HG. There was also a marginally significant association between 2D:4D and SBJ such that low 2D:4D participants jumped further than high 2D:4D participants. Sit and reach and mod SR showed an advantage for girls, and there were positive but non-significant associations between 2D:4D and SR and mod SR in boys. In girls there were no significant relationships between 2D:4D and performance. 3.4. 2D:4D and body size and composition As with performance, we performed a number of regression analyses, considered the sexes separately and also removed the effect of age (the influence of BMI was not removed). Table 4 shows standardised regression coefficients (b) for the relationships between 2D:4D and body variables. As with performance variables we forced the independent variables simultaneously into the regression analysis. This minimised the possibility of multicollinearity. For girls there were significant positive relationships for mass, stature, BMI, and waist circumference. Table 3 Six regression analyses showing the relationships (standardised regression coefficients, b) between 2D:4D and performance traits in boys and girls. The influence of age and BMI has been removed in each analysis. Boys
Girls
Trait
b
t
p
b
t
p
MSFT Age BMI
−0.06 0.23 −0.47
2.08 7.66 15.29
0.04 0.0001 0.0001
−0.01 0.23 −0.45
0.33 6.93 13.20
0.74 0.0001 0.0001
1 / 10 × 5 m Age BMI
−0.10 0.25 −0.28
3.25 7.81 8.79
0.001 0.0001 0.0001
−0.002 0.22 −0.24
0.07 6.07 6.59
0.94 0.0001 0.0001
HG Age BMI
−0.054 0.42 0.26
1.94 14.82 9.20
0.05 0.0001 0.0001
0.04 0.46 0.31
1.34 15.73 10.50
0.18 0.0001 0.0001
SBJ Age BMI
−0.053 0.30 −0.41
1.77 9.78 13.48
0.08 0.0001 0.0001
−0.048 0.31 −0.36
1.48 9.29 10.58
0.14 0.0001 0.0001
SR Age BMI
0.03 −0.19 −0.06
0.84 5.68 1.71
0.40 0.0001 0.09
0.015 −0.07 −0.006
0.43 2.03 0.18
0.70 0.04 0.86
1.49 0.07 2.85
0.14 0.94 0.004
0.023 0.11 0.11
0.65 3.04 3.08
0.52 0.002 0.002
Mod SR Age BMI
0.05 0.002 0.10
Fig. 1. The relationship between right 2D:4D and running speed (1 / 10 × 5 s) in 899 boys.
For boys, there were no significant associations between 2D:4D and body size or composition. 4. Discussion We have confirmed the sexual dimorphism in right 2D:4D among children, i.e. boys tended to have lower mean 2D:4D than girls. The effect size of this sex difference (d = + 0.38) was within the small to medium range (d = + 0.25–0.50) which is characteristic of 2D:4D in adults [28,29]. Research has suggested the sex difference in 2D:4D is apparent by as early as two years old [3,30]. The sex difference is thought to be the result of higher exposure to prenatal testosterone and lower oestrogen in the male foetus compared to the female which are exposed to lower testosterone and higher oestrogen, resulting in lower 2D:4D in males than in females [7]. With regard to sexual dimorphism in performance variables, we have found significant advantages for boys in aerobic capacity (MSFT), speed and agility (1 / 10 × 5 m), strength (HG) and power (SBJ) and for girls in flexibility (SR and mod SR). Considering 2D:4D in boys, there were negative correlations with MSFT (p = 0.04), 1 / 10 × 5 m (p = 0.001), HG (p = 0.05) and SBJ (p = 0.08) and non-significant positive correlations with flexibility (SR p = 0.40; mod SR p = 0.14). This pattern of relationships between 2D:4D and sexually and non-sexually dimorphic traits may arise when sexual dimorphism in performance is initially dependent on organisational responses to sex hormones in the foetus. Of course performance in such things as 10 × 5 m and HG may be modified by training. However, it is possible that early organisational effects of testosterone and oestrogen may influence sex differences and individual differences with regard to Table 4 Six regression analyses showing the relationships (standardised regression coefficients, b) between 2D:4D and body size and composition traits in boys and girls. The influence of age has been removed in each analysis. Boys
Girls
Trait
b
t
p
b
t
p
% fat Age Stature Age Mass Age BMI Age Leg length Age Waist Age
−0.015 0.18 −0.04 0.64 −0.03 0.43 −0.02 0.19 −0.05 0.56 −0.013 0.30
0.47 5.53 1.45 24.9 0.92 14.37 0.48 5.92 1.62 19.33 0.40 9.26
0.64 0.0001 0.15 0.0001 0.36 0.0001 0.63 0.0001 0.11 0.0001 0.69 0.0001
0.056 0.22 0.058 0.62 0.091 0.46 0.092 0.25 0.056 0.55 0.10 0.32
1.67 6.27 2.11 22.30 2.91 14.93 2.70 7.47 1.87 18.33 3.00 9.49
0.10 0.0001 0.04 0.0001 0.004 0.0001 0.007 0.0001 0.06 0.0001 0.003 0.001
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performance variables. With regard to 2D:4D in girls, there was little evidence for significant associations with any of the performance variables. Our findings represent the first investigation of 2D:4D and performance levels in boys and girls. They replicate some, but not all, reports of the links between 2D:4D and performance in adolescents and adults. (i) For sprinting speed Manning and Hill [31] reported that 2D:4D was negatively related to sprinting speed over 20 m, 30 m, 40 m & 50 m in a sample of teenage boys (girls were not considered). The effect size (r = 0.10 to r = 0.14) was similar to that which we report here for 10 × 5 m sprints. (ii) There is evidence that low 2D:4D is associated with HG strength in men but not women. Fink et al. [32] reported that low 2D:4D was associated with high HG in German and Mizos men, and in Chinese men [33] and similar findings were reported by Hone & McCullough [34] in students of mixed ethnicity from the USA. However, Zhao et al. [33] Hone and McCullough [34] and van Anders [35] reported no association between 2D:4D and hand grip strength in women. Thus, we feel that our data from children maps on to the adult data, such that low 2D:4D is linked to high HG in males but not females. (iii) When assessing aerobic fitness, we found that low 2D:4D was related to high performance in the MSFT in boys only. In adults there is evidence that speed in middle- and long-distance races is linked to low 2D:4D in both men and women [17]. In this regard there may be sex differences in the predictive power of 2D:4D in children compared to adults. One of the reasons for the differences may be that children are non-metabolic specialists therefore those children who perform well on endurance-based tasks, such as the MSFT are also likely to perform well on the 10 × 5 m test [36]. Nevertheless, this does not explain why there would be a relationship in boys but not girls. (iv) There were positive associations between 2D:4D and the SR and mod SR. This pattern differed from the negative associations seen for 2D:4D and 10 × 5 m, HG and MSFT. However, the correlations between 2D:4D and flexibility were not significant in boys or in girls. This suggests that 2D:4D is not predictive of children's performance in sports that involve high flexibility. Consistent with this, Peeters & Claessens [37] have reported that left hand 2D:4D does not predict performance in elite female gymnasts. Research has indicated that flexibility may be influenced by the hormone relaxin which has a role in ligament laxity in females [38]. However a study which examined the levels of serum relaxin in athletic populations showed no significant sex differences [39], but the links between relaxin levels and generalised joint laxity are limited. The findings of this study support the conclusions of Peeters et al. [20] who found that fitness is not related to a lower 2D:4D in girls. These similarities seem to exist despite some methodological differences in the study, which was based on data collected in 1979–1980 [20]. Digit ratio was measured using an X-ray of the left hand, as skeletal age was also determined using the Tanner–Whitehouse II method. However right-hand 2D:4D has consistently been shown to be a better indicator of prenatal androgenisation [29]. In addition, some of the measures of fitness that were used in the Flemish study have been shown to be affected by poor validity and reliability [40]. With regard to body size variables, we have found a number of positive correlations between 2D:4D and body size (stature, mass, BMI, and waist circumference) in girls but not boys. This is a surprising finding. A positive association between 2D:4D and BMI in males and females has been previously reported [41]. However, the associations were only found in the left hand 2D:4D in a relatively small sample size (n = 80); whereas, no significant relationships were reported between 2D:4D and various anthropometric measures in a large sample of adults (n = 14,916) [42]. In contrast, the present study found a significant positive relationship between high 2D:4D and high BMI in a large sample of children but the effects were confined to girls. There are public health concerns with rising levels of sedentary lifestyles, obesity and poor levels of fitness across the UK, which have been shown to track from childhood to adulthood [43,44]. Manning and Bundred [45] found
that males with a high 2D:4D were at the greatest risk of a heart attack due to lower levels of the male sex hormone testosterone, which is known to protect against heart attack (MI) and this finding has recently been supported in Chinese populations [46]; whereas markers of low-grade inflammation IL-6 which is linked with heart disease, was found to be positively associated with 2D:4D in girls [47]. A high 2D:4D does not suggest a causal link with a MI but may be a marker and could therefore be used as a risk factor [45]. Comparisons of the findings from the present study with previous studies are difficult due to the limited number of child studies. It is unclear whether 2D:4D changes as children develop into teenagers and then adults. However it has been suggested that 2D:4D is established early in development (before 2 years of age) [3]. One longitudinal study found that 2D:4D increased slightly with age [48]. However, the rank-order of 2D:4D remained the same, suggesting that relative 2D:4D within birth cohorts does not change with age, but the study had a low sample size (n = 108) and only consisted of Afro-Caribbean children, who have the lowest 2D:4D in comparison to other ethnic origins [30]. Our own data show that 2D:4D remained the same in children aged 8–12 years over a 12 month period (n = 250 boys; n = 228). Given that British girls achieve peak height velocity at 11.9 ± 0.7 years [49] this study would include measurements of 2D:4D during a period of significant growth, yet 2D:4D remained unchanged (t = 1.016; p = 0.310; CV = 1.3%). If 2D:4D is constant from birth, then the use of 2D:4D as a potential tool for talent identification may be possible. However, before such assumptions can be made a large prospective study following children from a young age through their competitive peak into adulthood would be required. Further research is required to determine whether prenatal testosterone exposure levels fully impact on performance in pre- or post-pubescent children and youths, therefore it is recommended to investigate the relationship between 2D:4D and health and fitness in post-pubertal youths and in elite and sub-elite athletic populations. We have found significant links between 2D:4D and aerobic fitness in boys and there has been a decline in the UK of aerobic fitness at a rate of 1.3% and 2.3% per year in boys and girls respectively from 1998–2010 [13]. It is likely that an increase in sedentary behaviour accounts for much of this decline. However, there may also be an influence on aerobic fitness via the developing foetus from the increasing use of endocrine distorters. Auger et al. [50] have shown that environmental levels of commonly used oestrogenic and anti-androgenic compounds feminize 2D:4D in male rats. Interestingly, this effect is long-lasting and has epigenetic consequences, as it is carried on in the unexposed male progeny. In conclusion the current study found significant relationships between a lower right hand 2D:4D and superior scores for aerobic capacity, speed and power in a large population of Welsh boys but not girls. These results suggest that prenatal levels of testosterone and oestrogen have organising effects on levels of speed, endurance and strength of boys. Future studies should examine whether training (and the frequency of training) affects the associations discussed in this paper. Conflict of interest The authors report no conflicts of interest. Funding This work was supported by grants from the Big Lottery Fund and by Denbighshire County Borough Council. Acknowledgments We would like to thank all the schools and children involved in the study and the F Factor research team (as well as the students at Glyndŵr
R. Ranson et al. / Early Human Development 91 (2015) 327–331
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Early Human Development journal homepage: www.elsevier.com/locate/earlhumdev
Digit ratio (2D:4D) and physical fitness (Eurofit test battery) in school children R. Ranson a, G. Stratton b,c, S.R. Taylor a,⁎ a b c
Sport & Exercise Sciences, Glyndwr University, Wrexham LL11 2AW, UK Applied Sports Technology Exercise and Medicine Centre (A-STEM), Swansea University, Swansea, UK School of Sport Exercise and Health Sciences, University of Western Australia, Crawley, WA 6160, Australia
a r t i c l e
i n f o
Article history: Received 30 November 2014 Received in revised form 23 February 2015 Accepted 16 March 2015 Keywords: 2D:4D Eurofit Children's fitness Testosterone Anthropometrics
a b s t r a c t Background: The relative lengths of the index finger to the ring finger (2D:4D) is sexually dimorphic and is thought to be a correlate of prenatal sex steroids (low 2D:4D = high prenatal testosterone and low prenatal oestrogen). In adults there have been reports that low 2D:4D is consistently associated with high sports performance. Aims: To investigate correlations between 2D:4D and fitness levels in children. Study design: Right 2D:4D and body size were measured, in addition to flexibility, speed, endurance and strength (Eurofit tests). Subjects: 922 boys and 835 girls (mean ages (years): 10.8 ± 1.01 and 10.07 ± 1.00 respectively). Outcome measures: height, mass, BMI, triceps and subscapular skinfolds, 20 m shuttle run, sit and reach, standing broad jump, hand grip strength, 10 × 5 m sprint, and the sit and reach test. Results: Boys significantly outperformed the girls in the 10 × 5 m sprints, the 20 m shuttle run, standing broad jump, and hand grip strength. In boys but not girls, 2D:4D was significantly negatively correlated with scores in all these tests except the standing broad jump. In girls but not boys, 2D:4D was significantly positively correlated to stature, mass, BMI and waist circumference. Conclusions: It is suggested that high prenatal testosterone and low prenatal oestrogen (low 2D:4D) is implicated in high sprinting speed, endurance and hand grip strength in boys. In girls low prenatal testosterone and high prenatal oestrogen is associated with large body size. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction The multifactorial nature of the male advantage in sport, and the sex differences in physique, are thought to be partly a result of prenatal effects of testosterone on the brain and/or on the cardiovascular system [1,2]. One correlate of prenatal testosterone is the relative lengths of the 2nd (index finger) and 4th (ring finger) digits (2D:4D) and the 2D:4D ratio is negatively related with prenatal testosterone and positively with prenatal oestrogen [3–5]. Many studies have shown that males generally have relatively shorter 2nd digits than 4th digits compared to females [6,7] which results in a lower, “more masculine” 2D:4D associated with higher prenatal testosterone levels [8]. The relative sizes of the fingers are established in utero and the ratio is reported to be stable during postnatal growth and throughout puberty [9,3]. Therefore, if 2D:4D remains relatively constant during life, and there is a relationship between 2D:4D and fitness or sporting ability, then the ratio may be useful as a talent identification tool [1,10]. The benefits of regular participation in physical activity throughout childhood are well documented [11]. However in recent years there ⁎ Corresponding author at: Glyndŵr University, Wrexham Campus, Mold Road, Wrexham LL11 2AW, UK. Tel.: +44 1978 293092. E-mail address: [email protected] (S.R. Taylor).
http://dx.doi.org/10.1016/j.earlhumdev.2015.03.005 0378-3782/© 2015 Elsevier Ireland Ltd. All rights reserved.
has been an increase in sedentary behaviour and a significant decline in aerobic fitness (average decline of 0.43% per year) in the child population [12]. Data from the UK show that aerobic fitness has declined at a rate of 1.3% and 2.3% per year in boys and girls respectively from 1998 to 2010 [13]. The Eurofit tests assess various principle components of physical fitness, both health- and skill-related fitness characteristics [14]. The Eurofit tests have been widely used due to their simple administration [15] and normative data that can detect status changes and trends. There are a number of studies into the relationship between 2D:4D and sport performance, although results have often been based on small sample sizes and have been performed on adult males [10]. A lower 2D:4D has been reported to be related to high achievements in the following: men's professional football, [1] and in a range of men's sports, [1] female athletic ability, [16] endurance running times for men and women [17], slalom skiing times for men and women [18], and rowing times for women [19] . A major limitation of 2D:4D and sporting ability studies in the literature, is that the evidence is often based on selection and rankings which are prone to several sources of bias such as selection effects based on game intelligence, resilience as well as subjective ‘views’ from coaches [10,17]. Research on the relationship between children's 2D:4D and health and fitness is limited. Of the available literature
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Hönekopp et al. [2] examined the relationship between 2D:4D and physical education (PE) grade in teenagers. The PE grade however reflects attainment levels in a variety of physical activities and not a specific measure of fitness. The attainment levels are therefore based on subjective rather than objective measures. In one of the only studies to objectively assess performance measures, Peeters et al. [20] examined the relationship between 2D:4D and health- and skill-related fitness in Flemish children and showed no relationship between digit ratio and various components of physical fitness. However, the study was limited to girls, who were aged 6–18 years and based on left hand 2D:4D and therefore has limited application, ideally the study should be repeated using the right or both hands [20]. To our knowledge there are no studies that have examined the relationship between 2D:4D and fitness in both boys and girls. If fitness is related to the effects of prenatal sex steroids we would expect that 2D:4D will be correlated with fitness in pre-pubertal children. Therefore, the purpose of this study was to examine the relationship between 2D:4D and healthand skill-related fitness tests in school children. It was predicted that children with a low 2D:4D would perform better in the Eurofit tests than children with high 2D:4D. 2. Methods 2.1. Participants and procedures The university Research Ethics Committee approved the study which involved 1776 Welsh school children recruited from primary and secondary schools aged 8–12 years (boys 10.1 ± 1.0 years; girls 10.1 ± 0.9 years). Almost all of the participants were Caucasian children (97%), with a few East Asian and Black children. Inclusion of all ethnicities made little difference to subsequent analyses. Therefore, we report results from the complete sample. Every school, parent/ guardian and pupil gave informed consent and assent respectively and had the right to withdraw. All fitness testing was performed on the same day of the week between 09:00 and 15:00 h. Participants undertook a standardised 10-minute warm up consisting of dynamic stretches to music. Right hand 2D:4D was measured using a digital camera (Sony Cyber-shot, Singapore) and Adobe Photoshop software (Adobe systems, San Jose, CA) following the procedures outlined by Ranson et al. [21]. All the photographs were coded to ensure that the researcher measuring digit length was blinded to the fitness scores and the appearance of the individual child to reduce experimenter bias [22]. BMI was calculated as body mass in kilogrammes divided by the square of stature in metres (kg/m2). Triceps and subscapular skinfolds were measured using Harpenden callipers (John Bull British Indicators, West Sussex, UK) to the nearest millimetre and per cent body fat (%BF) was calculated using the methods outlined by Lohman [23]. All children participated in the 20 m shuttle run (20MSFT) to measure aerobic fitness [24], sit and reach (SR) to quantify the level of flexibility, standing broad jump (SBJ), to examine leg power, hand grip strength (HG) to measure strength and the 10 × 5 m sprint (10 × 5 m) tests to test sprint performance [14]. An additional test was also administered; the modified sit and reach test (mod SR) was used to assess flexibility whilst taking into account limb length [25]. Participants were given a demonstration and a practice attempt before performing each test, and were encouraged throughout. The highest score was recorded for HG, SR, mod SR, and SBJ where the children had 3 attempts. All tests were administered by a trained member of the research team. 2.2. Statistical Analysis Descriptive statistics were calculated using Microsoft Excel (2007) and the statistical analyses were performed using IBM SPSS (v.19) software. Normality of the data was checked and Pearson's correlation and standardised linear regression coefficients were used to investigate
relationships between 2D:4D and the health and fitness scores. All data were tested for normality using Kolmogorov–Smirnov as the data set included more than 50 participants [26]. The data were corrected for age and BMI to normalise the data for the morphological changes that occur during adolescence. An alpha level of p ≤ 0.05 was used as the criterion to determine significance. 3. Results There were 1776 participants in the sample. However, not all participants were measured for all variables. Therefore, numbers per variable differed somewhat. Means (± SD) for age, stature and mass were as follows: boys, age n = 911, 10.08 ± 1.01 years; stature n = 917, 141.7 ± 8.51 cm; body mass n = 917, 37.1 ± 9.27 kg; girls age n = 814, 10.07 ± 1.00 years; stature, n = 827, 141.2 ± 9.59 cm; body mass n = 823, 37.4 ± 10.48 kg. 3.1. Repeatability of 2D:4D The lengths of the 2nd and 4th digits of the right hand were measured on two separate occasions, with the second measurements performed by the same measurer and blind to the first measurements in 50 participants (boys n = 25; girls n = 25). From these two sets of measurements 2D:4Da and 2D:4Db were calculated. The Pearson's correlation coefficients of 2D:4Da compared to 2D:4Db was high (r = 0.95), as was the intra-class correlation (r = 0.90), whereas the coefficient of variation (CV) was very low (0.9%) [21]. Therefore, we concluded that our measurements of 2D:4D reflected real betweenindividual differences. 3.2. Sex differences Boys had a significantly lower mean 2D:4D (n = 922, 0.939 ± 0.034) than girls (n = 834, 0.952 ± 0.034; t = 8.07, p b 0.0001). The digital ratio data were found to be normally distributed (Z = 0.019; p = 0.146) but age and BMI were found to deviate from the normal distribution (p b 0.05), however the data were included in the linear regression as it has been suggested that in large samples this is not a requirement [27]. We found significant sexual dimorphism in the performance variables (Table 1). Boys had higher scores in the MSFT, ran faster 1 / 10 × 5 m, jumped further in SBJ, and were stronger for HG. In the SR and the mod SR girls were more flexible than boys. With regard to body size and composition (Table 2) we found significant sexual dimorphism in % body fat and leg length such that in comparison to girls boys had lower % body fat and longer legs. 3.3. 2D:4D and performance Digit ratio was sexually dimorphic. In addition, we found that 2D:4D was weakly but significantly related to age (n = 1725, r = 0.05, p = 0.04) and BMI (n = 1741, r = 0.06, p = 0.02). Therefore, we performed
Table 1 The means (±SD) for sex differences in the performance variables. There is a significant male advantage in MSFT, 1 / 10 × 5 m, SBJ, HG, and PT and a significant female advantage in SR and mod SR. Note that, in order to reverse the sign of the results for 10 × 5 m we transformed the times (1 / 10 × 5 m). Test
Boys (n)
Boys Mean ± SD
Girls (n)
Girls Mean ± SD
t
p
MSFT 1 / 10 × 5 m SBJ HG SR Mod SR
872 899 912 916 915 913
39.06 ± 17.43 0.044 ± 0.004 138.92 ± 21.06 16.94 ± 4.47 14.22 ± 6.3 24.54 ± 5.62
782 815 832 831 828 830
28.96 ± 12.73 0.042 ± 0.004 128.97 ± 19.29 15.65 ± 4.27 19.16 ± 6.62 28.57 ± 6.29
13.33 10.67 10.26 6.15 15.96 14.10
0.0001 0.0001 0.0001 0.0001 0.0001 0.0001
R. Ranson et al. / Early Human Development 91 (2015) 327–331
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Table 2 The means (±SD) for sex differences in body size and body composition variables. Males had significantly lower % fat and longer legs than females. Trait
Boys (n)
Boys Mean ± SD
Girls (n)
Girls Mean ± SD
t
p
% fat Leg length Stature Mass BMI Waist
913 855 917 917 917 912
21.09 ± 8.63 70.50 ± 5.80 141.72 ± 8.51 37.13 ± 9.27 18.28 ± 3.13 62.79 ± 8.51
821 776 827 823 823 825
27.51 ± 6.74 69.55 ± 6.26 141.22 ± 9.59 37.46 ± 10.48 18.52 ± 3.48 62.48 ± 9.74
17.12 3.19 1.15 0.69 1.50 0.72
0.0001 0.002 0.25 0.49 0.14 0.47
a number of multiple regressions and considered the relationships between 2D:4D and performance in boys and girls separately, removing the influence of age and BMI (Table 3). Note that, in these regression analyses the independent variables were forced simultaneously into the analysis. This minimised the possibility of multicollinearity. For comparison purposes we changed the direction of the performance variable 10 × 5 m by transforming it to 1 /10 × 5 m. We found negative relationships between 2D:4D and four performance variables in boys. That is, in comparison to high 2D:4D boys, low 2D:4D boys ran faster in the 10 × 5 m (1 / 10 × 5 m: Fig. 1), completed more runs in the MSFT and had stronger HG. There was also a marginally significant association between 2D:4D and SBJ such that low 2D:4D participants jumped further than high 2D:4D participants. Sit and reach and mod SR showed an advantage for girls, and there were positive but non-significant associations between 2D:4D and SR and mod SR in boys. In girls there were no significant relationships between 2D:4D and performance. 3.4. 2D:4D and body size and composition As with performance, we performed a number of regression analyses, considered the sexes separately and also removed the effect of age (the influence of BMI was not removed). Table 4 shows standardised regression coefficients (b) for the relationships between 2D:4D and body variables. As with performance variables we forced the independent variables simultaneously into the regression analysis. This minimised the possibility of multicollinearity. For girls there were significant positive relationships for mass, stature, BMI, and waist circumference. Table 3 Six regression analyses showing the relationships (standardised regression coefficients, b) between 2D:4D and performance traits in boys and girls. The influence of age and BMI has been removed in each analysis. Boys
Girls
Trait
b
t
p
b
t
p
MSFT Age BMI
−0.06 0.23 −0.47
2.08 7.66 15.29
0.04 0.0001 0.0001
−0.01 0.23 −0.45
0.33 6.93 13.20
0.74 0.0001 0.0001
1 / 10 × 5 m Age BMI
−0.10 0.25 −0.28
3.25 7.81 8.79
0.001 0.0001 0.0001
−0.002 0.22 −0.24
0.07 6.07 6.59
0.94 0.0001 0.0001
HG Age BMI
−0.054 0.42 0.26
1.94 14.82 9.20
0.05 0.0001 0.0001
0.04 0.46 0.31
1.34 15.73 10.50
0.18 0.0001 0.0001
SBJ Age BMI
−0.053 0.30 −0.41
1.77 9.78 13.48
0.08 0.0001 0.0001
−0.048 0.31 −0.36
1.48 9.29 10.58
0.14 0.0001 0.0001
SR Age BMI
0.03 −0.19 −0.06
0.84 5.68 1.71
0.40 0.0001 0.09
0.015 −0.07 −0.006
0.43 2.03 0.18
0.70 0.04 0.86
1.49 0.07 2.85
0.14 0.94 0.004
0.023 0.11 0.11
0.65 3.04 3.08
0.52 0.002 0.002
Mod SR Age BMI
0.05 0.002 0.10
Fig. 1. The relationship between right 2D:4D and running speed (1 / 10 × 5 s) in 899 boys.
For boys, there were no significant associations between 2D:4D and body size or composition. 4. Discussion We have confirmed the sexual dimorphism in right 2D:4D among children, i.e. boys tended to have lower mean 2D:4D than girls. The effect size of this sex difference (d = + 0.38) was within the small to medium range (d = + 0.25–0.50) which is characteristic of 2D:4D in adults [28,29]. Research has suggested the sex difference in 2D:4D is apparent by as early as two years old [3,30]. The sex difference is thought to be the result of higher exposure to prenatal testosterone and lower oestrogen in the male foetus compared to the female which are exposed to lower testosterone and higher oestrogen, resulting in lower 2D:4D in males than in females [7]. With regard to sexual dimorphism in performance variables, we have found significant advantages for boys in aerobic capacity (MSFT), speed and agility (1 / 10 × 5 m), strength (HG) and power (SBJ) and for girls in flexibility (SR and mod SR). Considering 2D:4D in boys, there were negative correlations with MSFT (p = 0.04), 1 / 10 × 5 m (p = 0.001), HG (p = 0.05) and SBJ (p = 0.08) and non-significant positive correlations with flexibility (SR p = 0.40; mod SR p = 0.14). This pattern of relationships between 2D:4D and sexually and non-sexually dimorphic traits may arise when sexual dimorphism in performance is initially dependent on organisational responses to sex hormones in the foetus. Of course performance in such things as 10 × 5 m and HG may be modified by training. However, it is possible that early organisational effects of testosterone and oestrogen may influence sex differences and individual differences with regard to Table 4 Six regression analyses showing the relationships (standardised regression coefficients, b) between 2D:4D and body size and composition traits in boys and girls. The influence of age has been removed in each analysis. Boys
Girls
Trait
b
t
p
b
t
p
% fat Age Stature Age Mass Age BMI Age Leg length Age Waist Age
−0.015 0.18 −0.04 0.64 −0.03 0.43 −0.02 0.19 −0.05 0.56 −0.013 0.30
0.47 5.53 1.45 24.9 0.92 14.37 0.48 5.92 1.62 19.33 0.40 9.26
0.64 0.0001 0.15 0.0001 0.36 0.0001 0.63 0.0001 0.11 0.0001 0.69 0.0001
0.056 0.22 0.058 0.62 0.091 0.46 0.092 0.25 0.056 0.55 0.10 0.32
1.67 6.27 2.11 22.30 2.91 14.93 2.70 7.47 1.87 18.33 3.00 9.49
0.10 0.0001 0.04 0.0001 0.004 0.0001 0.007 0.0001 0.06 0.0001 0.003 0.001
330
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performance variables. With regard to 2D:4D in girls, there was little evidence for significant associations with any of the performance variables. Our findings represent the first investigation of 2D:4D and performance levels in boys and girls. They replicate some, but not all, reports of the links between 2D:4D and performance in adolescents and adults. (i) For sprinting speed Manning and Hill [31] reported that 2D:4D was negatively related to sprinting speed over 20 m, 30 m, 40 m & 50 m in a sample of teenage boys (girls were not considered). The effect size (r = 0.10 to r = 0.14) was similar to that which we report here for 10 × 5 m sprints. (ii) There is evidence that low 2D:4D is associated with HG strength in men but not women. Fink et al. [32] reported that low 2D:4D was associated with high HG in German and Mizos men, and in Chinese men [33] and similar findings were reported by Hone & McCullough [34] in students of mixed ethnicity from the USA. However, Zhao et al. [33] Hone and McCullough [34] and van Anders [35] reported no association between 2D:4D and hand grip strength in women. Thus, we feel that our data from children maps on to the adult data, such that low 2D:4D is linked to high HG in males but not females. (iii) When assessing aerobic fitness, we found that low 2D:4D was related to high performance in the MSFT in boys only. In adults there is evidence that speed in middle- and long-distance races is linked to low 2D:4D in both men and women [17]. In this regard there may be sex differences in the predictive power of 2D:4D in children compared to adults. One of the reasons for the differences may be that children are non-metabolic specialists therefore those children who perform well on endurance-based tasks, such as the MSFT are also likely to perform well on the 10 × 5 m test [36]. Nevertheless, this does not explain why there would be a relationship in boys but not girls. (iv) There were positive associations between 2D:4D and the SR and mod SR. This pattern differed from the negative associations seen for 2D:4D and 10 × 5 m, HG and MSFT. However, the correlations between 2D:4D and flexibility were not significant in boys or in girls. This suggests that 2D:4D is not predictive of children's performance in sports that involve high flexibility. Consistent with this, Peeters & Claessens [37] have reported that left hand 2D:4D does not predict performance in elite female gymnasts. Research has indicated that flexibility may be influenced by the hormone relaxin which has a role in ligament laxity in females [38]. However a study which examined the levels of serum relaxin in athletic populations showed no significant sex differences [39], but the links between relaxin levels and generalised joint laxity are limited. The findings of this study support the conclusions of Peeters et al. [20] who found that fitness is not related to a lower 2D:4D in girls. These similarities seem to exist despite some methodological differences in the study, which was based on data collected in 1979–1980 [20]. Digit ratio was measured using an X-ray of the left hand, as skeletal age was also determined using the Tanner–Whitehouse II method. However right-hand 2D:4D has consistently been shown to be a better indicator of prenatal androgenisation [29]. In addition, some of the measures of fitness that were used in the Flemish study have been shown to be affected by poor validity and reliability [40]. With regard to body size variables, we have found a number of positive correlations between 2D:4D and body size (stature, mass, BMI, and waist circumference) in girls but not boys. This is a surprising finding. A positive association between 2D:4D and BMI in males and females has been previously reported [41]. However, the associations were only found in the left hand 2D:4D in a relatively small sample size (n = 80); whereas, no significant relationships were reported between 2D:4D and various anthropometric measures in a large sample of adults (n = 14,916) [42]. In contrast, the present study found a significant positive relationship between high 2D:4D and high BMI in a large sample of children but the effects were confined to girls. There are public health concerns with rising levels of sedentary lifestyles, obesity and poor levels of fitness across the UK, which have been shown to track from childhood to adulthood [43,44]. Manning and Bundred [45] found
that males with a high 2D:4D were at the greatest risk of a heart attack due to lower levels of the male sex hormone testosterone, which is known to protect against heart attack (MI) and this finding has recently been supported in Chinese populations [46]; whereas markers of low-grade inflammation IL-6 which is linked with heart disease, was found to be positively associated with 2D:4D in girls [47]. A high 2D:4D does not suggest a causal link with a MI but may be a marker and could therefore be used as a risk factor [45]. Comparisons of the findings from the present study with previous studies are difficult due to the limited number of child studies. It is unclear whether 2D:4D changes as children develop into teenagers and then adults. However it has been suggested that 2D:4D is established early in development (before 2 years of age) [3]. One longitudinal study found that 2D:4D increased slightly with age [48]. However, the rank-order of 2D:4D remained the same, suggesting that relative 2D:4D within birth cohorts does not change with age, but the study had a low sample size (n = 108) and only consisted of Afro-Caribbean children, who have the lowest 2D:4D in comparison to other ethnic origins [30]. Our own data show that 2D:4D remained the same in children aged 8–12 years over a 12 month period (n = 250 boys; n = 228). Given that British girls achieve peak height velocity at 11.9 ± 0.7 years [49] this study would include measurements of 2D:4D during a period of significant growth, yet 2D:4D remained unchanged (t = 1.016; p = 0.310; CV = 1.3%). If 2D:4D is constant from birth, then the use of 2D:4D as a potential tool for talent identification may be possible. However, before such assumptions can be made a large prospective study following children from a young age through their competitive peak into adulthood would be required. Further research is required to determine whether prenatal testosterone exposure levels fully impact on performance in pre- or post-pubescent children and youths, therefore it is recommended to investigate the relationship between 2D:4D and health and fitness in post-pubertal youths and in elite and sub-elite athletic populations. We have found significant links between 2D:4D and aerobic fitness in boys and there has been a decline in the UK of aerobic fitness at a rate of 1.3% and 2.3% per year in boys and girls respectively from 1998–2010 [13]. It is likely that an increase in sedentary behaviour accounts for much of this decline. However, there may also be an influence on aerobic fitness via the developing foetus from the increasing use of endocrine distorters. Auger et al. [50] have shown that environmental levels of commonly used oestrogenic and anti-androgenic compounds feminize 2D:4D in male rats. Interestingly, this effect is long-lasting and has epigenetic consequences, as it is carried on in the unexposed male progeny. In conclusion the current study found significant relationships between a lower right hand 2D:4D and superior scores for aerobic capacity, speed and power in a large population of Welsh boys but not girls. These results suggest that prenatal levels of testosterone and oestrogen have organising effects on levels of speed, endurance and strength of boys. Future studies should examine whether training (and the frequency of training) affects the associations discussed in this paper. Conflict of interest The authors report no conflicts of interest. Funding This work was supported by grants from the Big Lottery Fund and by Denbighshire County Borough Council. Acknowledgments We would like to thank all the schools and children involved in the study and the F Factor research team (as well as the students at Glyndŵr
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