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Hematological-Hormonal and Fitness Indices in Youth Swimmers-Gender Related Comparisons
Hematological-Hormonal and Fitness Indices in Youth Swimmers-Gender Related Comparisons
2478/hukin-2019-0027 131
Section II ‐ Exercise Physiology & Sports Medicine
by
Guang Cai , Jun Qiu , Shuai Chen , Qile Pan1, Xunzhang Shen1, Jie Kang2
1 1 1
This study objective was to evaluate gender differences in hematological, hormonal and fitness variables among
youth swimmers and to explore relationships between erythrocyte indices and aerobic and anaerobic capacity. 137 girls
and 171 boys participated in the study and were divided into three groups based on their training experience. Blood
samples were obtained to determine red blood cell counts, hemoglobin concentration, hematocrit, and plasma
erythropoietin and testosterone levels. VO 2max was assessed using a submaximal cycle protocol. 76 girls and 102 boys
also undertook a Wingate test to determine their peak anaerobic power. Boys had higher (p < 0.05) means than girls for
all hematological variables except for erythropoietin and these variables demonstrated an increase with training in boys.
The average VO2max in l∙min-1 and peak anaerobic power in watts were also higher in boys (2.91 ± 0.08 and 547 ± 28,
respectively) than girls (2.25 ± 0.07 and 450 ± 26, respectively). Modest but significant (p < 0.05) correlations were
found between VO2max and red blood cell counts (r = 0.252), hemoglobin concentration (r = 0.345), or hematocrit (r =
0.345) and between peak anaerobic power and red blood cell counts (r = 0.304), hemoglobin concentration (r = 0.319) or
hematocrit (r = 0.351). This study revealed relatively lower yet age- and gender-appropriate hematological, hormonal
and fitness indices in youth swimmers. The gender-related differences in erythrocyte indices seem unrelated to
erythropoietin and may be explained by the higher testosterone levels seen in boys. Given their correlation to both
aerobic and anaerobic capacity, erythrocyte indices may be used as part of talent identification for sports.
Key words: erythrocytes, testosterone, aerobic capacity, anaerobic power, training.
Introduction
The primary role of red blood cells (RBCs) is been regarded as a key limiting factor to
to transport respiratory gases. Oxygen (O 2) maximum O2 uptake (V̇O2max), which predicts
brought into the pulmonary circulation is bound endurance performance. RBCs also fulfill a variety
by hemoglobin (Hb) via oxygenation. The of other functions such as buffering changes in
resulting oxyhemoglobin (Hb-O2) is then blood pH by transport of CO2 and by binding of
circulated by the cardiovascular system to the H+ to hemoglobin.
periphery where O2 is released from HB-O2 and It has long been found that endurance athletes
diffuses into tissue cells. The physiological as compared to untrained counterparts have
significance of O2 transport by Hb is well- hematological abnormalities and decreased Hb
illustrated by anemia where decreased Hb also levels near to or below the lower limit of the
decreases sports performance despite a normal range (Coates et al., 2016, Rietjens et al.,
compensatory increase in cardiac output (Eichner, 2002). Previous studies also demonstrated a
1992), and by a strong positive correlation decrease in RBCs, Hb, and mean corpuscular
between aerobic performance and total Hb volume (MCV) following an acute bout of intense
(Schmidt and Prommer, 2008). In fact, Hb has exercise (Cordova and Escanero, 1992; Yalcin et
al., 2003). Explanations for this deformation in
1
- Shanghai Research Institute of Sports Science, Shanghai, China.
2
- Department of Health and Exercise Science, The College of New Jersey, New Jersey, USA.
erythrocytes include expanded plasma volume, found that connect erythrocyte indices with
increased intravascular hemolysis, anaerobic performance.
gastrointestinal blood loss, and insufficient The aim of this study was to evaluate gender
dietary intake of iron. Most observations have differences in hematological and fitness variables
been carried out based on middle- and long- among youth swimmers and to explore
distance running in which oxidative energy relationships between erythrocyte indices and
transformation is critical to successful aerobic as well as anaerobic capacity. By
performance. stratifying study participants based on their
Much less is known regarding hematological training experience, we were also able to assess
profiles in children. In particular, there is a gender differences in hematological response to
paucity of literature regarding gender-differences training. We hypothesized that 1) boys would
in erythrocyte variables and how they may be demonstrate higher values than girls in
related to fitness of young athletes. Not only is the erythrocyte indices and aerobic and anaerobic
research in this area limited, but the existing capacity and 2) erythrocyte indices would be
evidence is also inconsistent. Boyadjiev and correlated to both aerobic and anaerobic capacity
Taralov (2000) observed gender differences in in youth swimmers. (朱镕鑫)
RBCs, Hb, and hematocrit (Hct) with boys
demonstrating higher values than girls. The same
Methods
research group also found lower RBC and Hb Participants
levels in pubescent swimmers and rowers as 308 youth swimmers including 137 girls and
compared to their control counterparts, which 171 boys aged 8 to 16 volunteered to participate in
suggests that erythrocyte indices may not this study. They typically trained six days a week
necessarily explain gains in fitness as children with each training session consisting of two hours
train. In contrary, Eastwood et al. (2009) revealed in water and a half hour on land. Both children
a positive correlation between VO2max and a total and their parents were informed of the purpose
quantity of Hb (Hbmass) in adolescent cyclists, and procedure of the study. While written consent
indicating that measuring variables related to was obtained from their parents, each child also
erythrocytes can serve as an indicator of aerobic gave their ascent to participate. The research
capacity. In this latter study, no gender protocol was approved by the Ethics Committee
comparisons were made due to a small sample of the Fudan University.
size. To assess gender differences in hematological
Given a direct correlation between VO 2 and response to training, participants within each
swimming velocity, VO2max is viewed as one of the gender were further divided into three groups
most relevant measure of functional capacity according to their training experience. The level of
among swimmers. It is considered that swimmers training was measured by their qualifying time in
with higher VO2max can sustain a large training swimming events. The following are the criteria
volume, swim faster and more economically, and used in forming the three groups:
recover faster (Pyne and Sharp, 2014; Toussaint Advanced - those who qualified to
and Hollander, 1994). In this context, it is compete at national-level competitions.
imperative that monitoring responses of Intermediate - those who qualified to
erythrocyte indices be carried out among compete at provincial-level competitions,
swimmers. Most swimming events last <2 Beginner - those who competed at various
minutes. Thus, training for swimming must also school- and district-level competitions.
emphasize developing anaerobic capacity. The gender- and training-specific physical
Children generally have limited anaerobic power and physiological characteristics of the
due to their under-developed muscle mass, participants are presented in Table 1.
neuromuscular coordination, and glycolytic Experimental procedure
ability (Bar-Or, 1987). Inbar and Bar-Or (1986) and Participants reported to the laboratory at ~8
Van Praagh (2000) reported no appreciable gender am after an overnight fast and at least 24 hours
gaps in anaerobic power in prepubescent
children. However, it is unclear if this is the case after their last training session. Body mass and
in youth athletes. In addition, no data has been height were measured using an electronic weight
Table 1
Physical characteristics of participants
Years of
Training Skeletal Age Body Mass
Gender Age (yr) Training Height (cm)
Experience (yr) (kg)
(yr)
Beginner
10.2 ± 1.8 10.3 ± 1.8 4.5 ± 1.9 146.8 ± 10.5 39.9 ± 9.1
(n = 93)
Intermediat
Girls (n = 37) 12.2 ± 1.3 11.8 ± 2.5 6.4 ± 1.8 159.8 ± 6.0 47.3 ± 7.8
e (n = 32)
Advanced
13.4 ± 1.1 13.3 ± 1.3 8.7 ± 1.6 166.9 ± 4.7 56.6 ± 6.1
(n = 12)
Beginner
10.5 ± 1.9 11.0 ± 1.9 4.7 ± 2.1 149.9 ± 12.0 43.8 ± 10.2
(n = 126)
Intermediat
Boys (n = 171) 12.9 ± 1.3 13.2 ± 1.5 7.3 ± 1.7 165.9 ± 10.1 54.8 ± 13.8
e (n = 37)
Advanced
14.2 ± 1.3 14.3 ± 1.4 7.1 ± 1.9 175.6 ± 3.6 61.7 ± 5.6
(n = 8)
Note: Data are means ± SD.
Table 2
Comparisons of hematological and hormonal variables with respective reference ranges of normal adults
Variables Gender Training Experience Means ± SD Reference Range*
Beginner 4.66 ± 0.28
Girls Intermediate 4.64 ± 0.28 4.2-5.4
Advanced 4.70 ± 0.30
RBC (×1012∙l-1)
Beginner 4.82 ± 0.31
Boys Intermediate 4.96 ± 0.31 4.7-6.1
Advanced 5.21 ± 0.27
Beginner 13.44 ± 0.72
Girls Intermediate 13.57 ± 0.81 11-15
Advanced 13.68 ± 0.77
Hb (g∙dl-1)
Beginner 13.74 ± 0.88
Boys Intermediate 14.41 ± 0.96 12-17
Advanced 15.46 ± 0.72
Beginner 40.30 ± 2.10
Girls Intermediate 41.01 ± 2.38 34.9-44.5
Advanced 41.35 ± 2.34
Hct (%)
Beginner 41.27 ± 2.45
Boys Intermediate 43.39 ± 2.81 38.8-50
Advanced 46.51 ± 1.99
Beginner 87.74 ± 3.69
Girls Intermediate 88.36 ± 3.49 79-101
Advanced 88.00 ± 1.84
MCV (fl)
Beginner 85.55 ± 3.52
Boys Intermediate 87.49 ± 3.44 79-101
Advanced 89.38 ± 2.92
Beginner 8.39 ± 3.97
Girls Intermediate 8.40 ± 3.92 2.6-18.5
Advanced 9.27 ± 4.50
EPO (mIU∙ml-1)
Beginner 7.77 ± 2.95
Boys Intermediate 8.80 ± 3.73 2.6-18.5
Advanced 7.42 ± 1.54
Beginner 32.10 ± 32.81
Girls Intermediate 49.32 ± 17.31 10-100
Advanced 53.69 ± 22.77
TST (ng∙dl-1)
Beginner 91.41 ± 146.94
Boys Intermediate 289.43 ± 183.73 270-1000
Advanced 468.09 ± 166.89
Note: RBC = Red blood counts; Hb = Hemoglobin; Hct = Hematocrit; MCV = Mean
corpuscular volume; EPO = Erythropoietin; TST = Testosterone. *Values were plasma
concentrations based on standard laboratory tests provided by Bechman Inc.
Table 3
Comparisons of hematological, hormonal and fitness variables between boys and girls
Variables Gender N Mean SE F ratio p
RBC Girls 137 4.668 0.035
39.249 0.000**
(×1012∙l-1) Boys 171 4.996 0.039
Hb Girls 137 13.551 0.098
44.133 0.000**
(g∙dl-1) Boys 171 14.535 0.111
Hct Girls 137 40.861 0.281
45.440 0.000**
(%) Boys 171 43.715 0.317
MCV Girls 137 87.574 0.414
0.018 0.895
(fl) Boys 171 87.491 0.467
EPO Girls 137 8.601 0.414
0.862 0.354
(mIU∙ml-1) Boys 171 8.021 0.467
TST Girls 137 44.716 14.002
127.652 0.000**
(ng∙dl-1) Boys 171 283.394 15.818
VO2max Girls 137 2.25 0.07
34.788 0.000**
(l∙min-1) Boys 171 2.91 0.08
VO2max Girls 137 47.53 1.85
5.87 0.016*
(ml∙kg-1∙min-1) Boys 171 54.27 2.08
WAnTpeak Girls 75 449.53 25.65
6.569 0.011*
(W) Boys 102 546.95 28.05
WAnTpeak Girls 75 8.96 50.12
2.106 0.149
(W/kg) Boys 102 9.97 54.81
Note: RBC = Red blood counts; Hb = Hemoglobin; Hct = Hematocrit; MCV = Mean
corpuscular volume; EPO = Erythropoietin; TST = Testosterone.
*p < 0.05; **p < 0.01.
Table 4
Correlation coefficients between hematological variables and aerobic and anaerobic
power in boys and girls combined
12 Hb Hct MCV EPO TST
RBC (x10 /L)
(g/dL) (%) (fl) (mIU/ml) (ng/dl)
VO2max
(l∙min-1) 0.252** 0.345** 0.345** 0.111* -0.047 0.452**
(N = 308)
WAnTpeak
(W) 0.304** 0.319** 0.351** 0.066 0.052 0.399*
(N = 178)
Note: RBC = Red blood counts; Hb = Hemoglobin; Hct = Hematocrit; MCV = Mean
corpuscular volume; EPO = Erythropoietin; TST = Testosterone, VO 2max = Maximum
oxygen uptake; WAnTpeak = Peak anaerobic power.
*p < 0.05; **p < 0.01.
p<0.05
p<0.05
p<0.05
Figure 1
Comparisons of red blood cell counts (RBCs), hemoglobin concentrations (Hb),
and hematocrits (Hct) between boys and girls stratified by their training level.
Values are means ± SE. Note: There were significant (p < 0.05) increases in RBCs,
Hb, and Hct in boys, but not in girls.
p<0.05
Figure 2
Comparisons of serum EPO and testosterone concentrations between boys
and girls stratified by their training level.
Values are means ± SE. Note: There was a significant (p < 0.05) increase in TST
in boys, but not in girls.
that the mean EPO recorded over a 24-h period 1986; Van Praagh, 2000). The gender gap in
was not correlated to training status or VO2max WAnTpeak found presently corroborates our
(Klausen et al., 1993). Although the major function findings of TST, which suggests that strength
of EPO is to stimulate erythropoiesis, the gains may respond to training more favorably in
production of EPO is thought to be mainly boys than girls.
induced by exposure to a hypoxic environment In the present study, modest but
(Mairbäurl, 2013), which is not the case in the significant positive correlations (i.e., r ≈ 0.25-0.35)
present study as our participants had all been were observed between VO2max and red blood cell
trained at sea level. Of interest is that EPO and variables including RBCs, Hb, and Hct (Table 4).
testosterone responded differently and there was Given that the primary role of red blood cells is to
virtually no correlation (i.e., r = 0.005) between transport O2 to the working tissue, these findings
these two variables. It has long been thought that make sense physiologically. Our findings are
testosterone stimulates erythropoiesis via its consistent with those of Eastwood et al. (2009)
stimulatory effect on EPO release (Shahani et al., who also revealed a positive correlation between
2009). However, this notion does not seem to VO2max and Hbmass in adolescent cyclists.
corroborate our current findings. The discordance Interestingly, significant correlations of similar
between the two hormones was also illustrated in magnitude (r ≈ 0.30-0.35) were also found
a recent study where a transdermal testosterone between WAnTpeak and the erythrocyte indices.
treatment for 3 years significantly increased This correlation may be explained by TST that can
hemoglobin, but not EPO levels (Maggio et al., cause parallel gains in both erythrocytes and
2013). muscle strength. As mentioned earlier, TST
Both absolute (l∙min-1) and relative (ml∙kg- stimulates erythropoiesis, while also enhances
1 -1
∙min ) VO2max were higher in boys than girls, protein synthesis. From a practical perspective,
although the difference in relative VO2max was our findings provided additional support for
much smaller (Table 3). Our VO 2max values were using erythrocyte indices, i.e., Hb or Hbmass, as
similar to those reported in untrained children of part of talent identification for sports. It has been
similar age. For example, Kemper et al. (2013) shown that endurance athletes have higher Hb mass
observed an average of VO2max of 2.3-2.5 for girls than non-endurance or untrained counterparts
and 2.6-2.8 l∙min-1 for boys aged 12-13, whereas and their Hb contents are relatively stable upon
our values were 2.3 and 2.9 l∙min -1, respectively. reaching puberty (Eastwood et al., 2009; Prommer
As for anaerobic capacity, gender differences in et al., 2008; Ulrich et al., 2011).
absolute (i.e., watts) WAnTpeak also existed with A potential limitation of this study is that
boys demonstrating higher values than girls we did not assess children’s maturity and
(Table 3). This gender difference was, however, grouping was made based on their training
largely abolished when WAnTpeak was normalized experience. As such, how many children were
to body mass (i.e., W∙kg-1) (Table 3). Gender pre-pubertal or pubertal within each group
differences were also reported by Bencke et al. remains unknown. As both puberty and
(2002) who used youth swimmers of similar age menstruation can affect blood-borne variables
range. Their WAnTpeak results, however, were especially those that are growth-related such as
somewhat lower than ours. For example, in their TST, our results should be interpreted with
study the average WAnTpeak were 339 W for girls caution.
and 355 W for boys, whereas our values were 449 In conclusion, this study revealed
W and 547 W, respectively. This difference may be relatively lower yet age- and gender-appropriate
explained in part by the fact that the brake erythrocyte indices and aerobic and anaerobic
resistance that we chose was slightly higher, i.e., capacity in youth swimmers with boys
75 vs. 68-70 g∙kg-1, although other factors such as demonstrating higher values than girls in most of
the condition of athletes cannot be ruled out. these variables. There were significant training-
WAnTpeak values for normal children aged from 7 induced increases in erythrocyte indices in boys,
to 14 have been reported to range from 250 to 500 but not in girls. The gender differences in
W with no appreciable erythrocyte indices seem unrelated to EPO and
may be explained by the higher plasma
testosterone levels seen in boys. Given their
gender gaps before puberty (Inbar and Bar-Or, correlation to both aerobic and anaerobic capacity,
Acknowledgements
Both Guang Cai and Jun Qiu are the co-leaders of this project. This work was supported by the “Key
Basic Research Grants” from Science and Technology Commission of Shanghai Municipality (Grant no
16JC1400500, 18DZ1200600, and 19DZ1200700), and partly supported by the “Science & Technology in 2017”
from Shanghai Sports Bureau (Project no. 17J008). The funders had no role in the study design, data
collection and analysis, decision to publish, or preparation of the manuscript. (刘旭)
References
Åstrand I. Aerobic work capacity in men and women with special reference to age. Acta Physiol Scand, 1960;
49: 1-92
Åstrand PO and Ryhming I. A nomogram for calculation of aerobic capacity (physical fitness) from pulse
rate during sub-maximal work. J Appl Physiol, 1954; 7: 218-221
Bar-Or O. The Wingate Anaerobic Test an Update on Methodology, Reliability and Validity. Sports Med,
1987; 4: 381–394
Bencke J, Damsgaard R, Saekmose A, Jørgensen P, Jørgensen K, Klausen K. Anaerobic power and muscle
strength characteristics of 11 years old elite and non-elite boys and girls from gymnastics, team
handball, tennis and swimming. Scand J Med Sci Sports, 2002; 12: 171-178
Biancotti PP, Caropreso A, Di Vincenzo GC, Ganzit GP, Gribaudo CG. Hematological status in a group of
male athletes of different sports. J Sports Med Phys Fit, 1992; 32: 70–75
Borges GF, Rama LM, Pedreiro S, Rosado F, Alves F, Santos AM, Paiva A, Teixeira AM. Hematological
changes in elite kayakers during a training season. Appl Physiol Nutr Metab, 2012; 37: 1140-1146
Boyadjiev N, Taralov Z. Red blood cell variables in highly trained pubescent athletes: a comparative
analysis. Br J Sports Med, 2000; 34: 200-204
Cai G, Shen XZ, Xu WY, Liang PZ. Relations between physical components and capacities of athletes of
different events. J Phys Ed, 2010; 17: 96-100
Coates A, Mountjoy M, Burr J. Incidence of Iron Deficiency and Iron Deficient Anemia in Elite Runners and
Triathletes. Clin J Sport Med. 2017; 27: 493-498
Cordova MA, Escanero JF. Iron, transferrin, and haptoglobin levels after a single bout of exercise in men.
Physiol Behav, 1992; 51: 719–722
Eastwood A, Bourdon PC, Withers RT, Gore CJ. Longitudinal changes in hemoglobin mass and VO 2max in
adolescents. Eur J Appl Physiol, 2009; 105: 715-721
Eichner ER. Sports anemia, iron supplements, and blood doping. Med Sci Sports Exerc, 1992; 24: S315–S318
Hero M, Wickman S, Hanhijarvi R, Siimes MA, Dunkel L. Pubertal upregulation of erythropoiesis in boys is
determined primarily by androgen. J Pediatr, 2005; 146: 245-252
Inbar O, Bar-Or O. Anaerobic characteristics in male children and adolescents. Med Sci Sports Exerc, 1986; 18:
264-269
Kemper HCG, Twisk JWR, Mechelen W. Changes in aerobic fitness in boys and girls over a period of 25
years: data from the Amsterdam Growth and Health Longitudinal Study Revisited and Extended.
Pediatr Exerc Sci, 2013; 25: 524-535
Klausen T, Dela F, Hippe E, Galbo H. Diurnal variations of serum erythropoietin in trained and untrained
subjects. Eur J Appl Physiol, 1993; 67: 545-548
Koch G, Röcker L. Plasma volume and intravascular protein masses in trained boys and fit young men. J
Appl Physiol, 1977; 43: 1085-1088
Maggio M, Snyder PJ, Cedi GP, Milaneschi Y, Luci M, Cattabiani C, Masoni S, Vignali A, Volpi R, Lauretani
F, Peachey H, Valenti G, Cappola AR, Longo D, Ferrucci L. Is the hematopoietic effect of testosterone
mediated by erythropoietin? The results of a clinical trial in older men. Andrology, 2013; 1: 24-28
Mairbäurl H. Red blood cells in sports: effects of exercise and training on oxygen supply by red blood cells.
Front Physiol, 2013; 4: 332
Mayr A, Kuipers H, Falk M, Santer P, Wierer B. Comparison of hematologic data in world elite junior speed
skaters and in non-athletic juniors. Int J Sports Med, 2006; 27: 283-288
Oski FA. Differential diagnosis of anemia. In: Hematology of Infancy and Childhood. 4th ed. Nathan DG and
Oski FA. Eds. Philadelphia: Saunders, 346-353; 1993
Prommer N, Sottas PE, Schoch C, Schumacher YO, Schmidt W. Total hemoglobin mass: a new parameter to
detect blood doping? Med Sci Sports & Exerc, 2008; 40: 2112–2118
Pyne DB, Sharp RL. Physical and energy requirements of competitive swimming events. Int J Sport Nutr
Exerc Metab. 2014; 24: 351-359Rietjens GJ, Kuiper H, Hartgens F, Keizer HA. Red blood cell profile of
elite Olympic distance triathletes. A three-year follow-up. Int J Sports Med, 2002; 23: 391-396
Schmidt W, Prommer N. Effects of various training modalities on blood volume. Scand J Med Sci Sports, 2008;
18: 57-69
Shahani S, Braga-Basaria M, Maggio M, Basaria S. Androgens and erythropoiesis: past and present. J
Endocrinol Invest, 2009; 32: 704-716
Toussaint HM, Hollander AP. Energetics of competitive swimming. Implications for training programmes.
Sports Med, 1994; 18: 384-405
Ulrich G, Bartech P, Friedmann-Bette B. Total hemoglobin mass and red blood cell profile in endurance-
trained and non-endurance-trained adolescent athletes. Eur J Appl Physiol, 2011; 111: 2855-2864
Van Praagh E. Development of anaerobic function during childhood and adolescence. Pediatr Exerc Sci, 2000;
12: 150-173
Yalcin O, Erman A, Muratli S, Bor-Kucukatay M, Baskurt OK. Time course of hemorheological alterations
after heavy anaerobic exercise in untrained human subjects. J Appl Physiol, 2003; 94: 997-1002
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