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Original article
Hormonal responses to a 160-km race across frozen
Alaska
W J Kraemer,1 M S Fragala,1 G Watson,1 J S Volek,1 M R Rubin,1 D N French,1
C M Maresh,1 J L Vingren,1 D L Hatfield,1 B A Spiering,1 J Yu-Ho,1 S L Hughes,2
H S Case,2 K J Stuempfle,3 D R Lehmann,4 S Bailey,5 D S Evans6
1
Human Performance
Laboratory, University of
Connecticut, Storrs,
Connecticut, USA; 2 McDaniel
College, Westminster, Maryland,
USA; 3 Gettysburg College,
Gettysburg, Philadelphia, USA;
4
Sitka Medical Center, Sitka,
Arkansas, USA; 5 Elon
University, Elon, North Carolina,
USA; 6 Alaska Native Medical
Center, Anchorage, Alaska, USA
Correspondence to:
Professor W J Kraemer, PhD,
University of Connecticut,
Human Performance Laboratory,
Storrs, Connecticut 06269-1110,
USA; william.kraemer@uconn.
edu
Accepted 12 June 2007
Published Online First
30 July 2007
ABSTRACT
Background: Severe physical and environmental stress
seems to have a suppressive effect on the hypothalamic–
pituitary–gonadal (HPG) axis in men. Examining hormonal
responses to an extreme 160-km competition across
frozen Alaska provides a unique opportunity to study this
intense stress.
Objective: To examine hormonal responses to an ultraendurance race.
Methods: Blood samples were obtained from 16 men
before and after racing and analyzed for testosterone,
interleukin-6 (IL-6), growth hormone (GH) and cortisol. Six
subjects (mean (SD) age 42 (7) years; body mass 78.9
(7.1) kg; height 1.78 (0.05) m raced by bicycle (cyclists)
and 10 subjects (age 35 (9) years; body mass 77.9
(10.6) kg; height, 1.82 (0.05) m) raced by foot (runners).
Mean (SD) finish times were 21.83 (6.27) and 33.98
(6.12) h, respectively.
Results: In cyclists there were significant (p(0.05)
mean (SD) pre-race to post-race increases in cortisol
(254.83 (135.26) to 535.99 (232.22) nmol/l), GH (0.12
(0.23) to 3.21 (3.33) mg/ml) and IL-6 (2.36 (0.42) to
10.15 (3.28) pg/ml), and a significant decrease in
testosterone (13.81 (3.19) to 5.59 (3.74) nmol/l).
Similarly, in runners there were significant pre-race to
post-race increases in cortisol (142.09 (50.74) to 452.21
(163.40) ng/ml), GH (0.12 (0.23) to 3.21 (3.33) mg/ml)
and IL-6 (2.42 (0.68) to 12.25 (1.78) pg/ml), and a
significant decrease in testosterone (12.32 (4.47) to 6.96
(3.19) nmol/l). There were no significant differences in
the hormonal levels between cyclists and runners
(p.0.05).
Conclusions: These data suggest a suppression of the
hypopituitary–gonadal axis potentially mediated by
amplification of adrenal stress responses to such an ultraendurance race in environmentally stressful conditions.
Both endurance training and acute endurance
exercise seem to have a suppressive effect on the
hypothalamic–pituitary–gonadal (HPG) axis in
men. For example, lower basal circulating levels
of testosterone have been reported in men who
have performed chronic endurance exercise for
many years.1 Additionally, in an acute longduration event such as a marathon2–5 or wrestling
tournament, in which athletes undergo extreme
physical stress,6 testosterone levels have been
shown to decrease. These observed decreases in
testosterone are typically seen when events exceed
3 h in duration,7 and remain decreased for up to
48 h.7 However, the cause of the decreased androgen levels is not completely understood. It is
possible that these reduced levels of testosterone
116
result from training-induced adaptations in the
hypothalamic–pituitary axis at the central (that is,
hypothalamus or pituitary) and/or peripheral (that
is, disrupted testicular function) levels by alterations in the negative feedback loop that regulates
production.8–10 Testosterone production in the
testes is primarily regulated by pituitary luteinising
hormone (LH) produced in the pituitary. During
marathon running and prolonged exercise, LH
levels have been shown both to decrease4 11 and
to remain unchanged.2 3 12 13 This discrepancy may
be due to the pulsatile release of LH.
Furthermore, during ultra-endurance events
stress hormones such as cortisol have been shown
to significantly increase above baseline levels14 15
possibly caused by the onset of hypoglycaemia.16
Additionally, cortisol seems to be positively correlated with the duration of exercise.17 Cortisol may
interfere with testosterone production, either
acutely during an endurance event or chronically
as a result of training. Cortisol production is
stimulated by interleukin (IL)-6, a cytokine produced by contracting muscles during exercise to
induce lipolysis, which may play a role in the
testosterone production pathway. Growth hormone (GH) is released from the anterior pituitary
gland during aerobic exercise.18 19 Like cortisol, GH
release seems to be positively correlated with the
duration of exercise.17 Although the primary
function of GH is to stimulate growth, it plays
an important role during endurance exercise in
increasing fat mobilisation and decreasing carbohydrate metabolism.
Environmentally cold conditions present an
additional stress to humans in maintaining
thermoneutral internal temperatures. Hormones
play an important role in thermoregulation.20
Thyroid hormones and noradrenaline are the
hormones most responsible for the maintenance
of the body’s internal temperature in response to
cold conditions,20 but other hormones play a role in
the physiological responses to this specific stress.
During cold exposure, GH secretion is suppressed21 22 and cortisol secretion is increased if
the exposure presents an adequate stress on the
body,23–25 whereas circulating testosterone is not
changed.
The combined stress of the duration of an ultraendurance event and the environmental stress of
the cold has previously been shown to reduce
serum sodium levels and haematocrit and plasma
arginine, vasopressin and serum aldosterone.26
Furthermore, the opioid receptor system seems to
Br J Sports Med 2008;42:116–120. doi:10.1136/bjsm.2007.035535
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Original article
regulate the physiological responses to exercise in thermally
stressful environments.27 Nevertheless, responses of GH, cortisol
and testosterone to these contradicting stresses is unknown and
presents a unique summated stress to the athlete.
We examined an ultra-endurance race to evaluate pre-race and
post-race responses of these hormones in endurance-trained
athletes in the Susitna 100 race (formerly called the Iditasport
100). This is a 160-km human-powered (running or cycling) ultraendurance race through the frozen wilderness in Alaska spanning
an elevation gain of over 2000 m in freezing ambient temperatures while carrying survival gear. Prior research on this event has
documented the physiological stress of this event. During this race
athletes lose significant amounts of weight, comsume about
30 864 kJ of energy and experience hyponatraemia, decreased
serum sodium, ketonuria and proteinuria.26 28 29 Not only does the
race put these athletes through extreme physical stress during the
race, but training for this extremely long event is rigorous,
providing a unique opportunity to evaluate chronic hormonal
adaptations and how these hormones respond to such extreme
physical and environmental stress.
METHODS
Subjects
All 122 entrants in the 2000 Susitna 100 Human Powered UltraMarathon were invited to participate in the study at the
mandatory informational meeting held 2 days before the race.
In total, 16 male athletes (10 runners and 6 cyclists) from
various parts of the USA volunteered to be subjects and signed a
written consent document approved by the university internal
review board. Each subject had understood the challenges of the
race, and owing to the fact that acclimatisation is not a factor,
had the clothing necessary for the race and also had travelled to
the site before the race to allow for adequate preparation. Each
had prepared for this ultra-endurance event. Owing to the field
testing nature of the study to determine hormonal (primarily
testosterone) levels in a field study, no geographical data or
training data were collected.
Design
All pre-race measurements were made 2 days before the race at
the informational meeting. Samples were obtained at a meeting
the day prior to the race to approximate the same circadian time
frame for their finishes. The cyclists and runners completed the
same 160-km (100-mile) snow-packed course, which wound
through the Alaskan wilderness and included an elevation gain of
2270 m. Ambient temperatures during the race ranged from 28uC
to 4uC and wet snow fell a few hours after starting the race. Five
checkpoints were located approximately every 15–20 miles (24–
32 km), where food and fluid were available. In addition, athletes
were required to carry 7 kg (15 lbs) of mandatory equipment at all
times, including two litres of fluid in an insulated container and
3000 kcal of food, which was predominately (60%) carbohydrate.
Post-race measurements were made within 15 minutes of each
athlete completing the race.
Body weight and plasma volume changes
Pre-race and post-race weight was measured using the Tanita
Body Fat Monitor/Scale (TBF-622), accurate to ¡0.1 kg. Pre-race
and post-race blood samples were collected by routine venepuncture, with athletes in a sitting position. Duplicate haematocrits
were measured immediately on the samples using standard
procedures from which changes in plasma volume were calculated
according to the formula of van Beaumont:30
Br J Sports Med 2008;42:116–120. doi:10.1136/bjsm.2007.035535
percentage change in plasma volume = (100/1002hematocritpre)
6100 (hematocritpre2hematocritpost)/hematocritpost,
where hematocritpre and hematocritpost are pre-race and postrace hematocrit samples, respectively.
Hormone analyses
Growth hormone was measured in duplicate using a double
antibody 125I radioimmunoassay (Nichols Institute Diagnostics,
San Juan, Capistrano, California, USA) from serum that was
obtained by centrifugation in Vacutainer serum separator tubes
(Becton Dickinson and Co, Franklin Lakes, New Jersey, USA),
frozen immediately on dry ice and stored at 220uC until thawed
for analysis. Intra-assay variance was 4.5 (1.2)%. Circulating
testosterone and cortisol were measured in duplicate using
commercially available enzyme immunoassays (Diagnostics
Systems Laboratories Inc., Webster, Texas, USA) from EDTAanticoagulated plasma that was obtained by centrifugation in
Vacutainer tubes, frozen immediately on dry ice and stored at
220uC until thawed for analysis. Intra-assay variance was 4.8
(1.3)% and 5.2 (1.2) for testosterone and cortisol, respectively.
IL-6 was measured in duplicate using a quantitative sandwich
enzyme immunoassay technique (R&D Systems Inc.,
Minneapolis, Minnesota, USA) from EDTA-anticoagulated
plasma that was obtained by centrifugation in Vacutainer tubes,
frozen immediately on dry ice and stored at 220uC until thawed
for analysis. Intra-assay variance was 7.4 (2.2)%.
Statistical analyses
A one-way analysis of variance was used to evaluate whether
differences in concentrations of growth hormone, IL-6, testosterone and cortisol existed pre-race between cyclists and
runners, and to determine if any significant changes between
pre-race and post-race concentrations of growth hormone, IL-6,
testosterone and cortisol differed by method of transport.
Pearson correlation analysis was used to determine relationships
between pre-race cortisol and testosterone and post-race cortisol
and testosterone. Using the nQuery Advisor software
(Statistical Solutions, Saugus, Massachusetts, USA) the statistical power for the numbers used ranged from 0.75 to 0.92.
Statistical significance was set at p(0.05.
RESULTS
The physical characteristics and race results for the runners and
cyclists are presented in table 1. Subjects lost significant
(p = 0.008) body mass between pre-race (mean (SD) 78.52
(8.32) kg) and post-race testing (76.91 (7.60) kg) corresponding
to 2.05% body mass loss. There was no significant (p = 0.102)
change in plasma volume.
No significant differences were found in the hormone levels
between the cyclists and runners before and after the race. The
results pre-race to post-race can be seen in table 2. Figure 3
shows mean pre-race and post race levels of testosterone, GH,
IL-6 and cortisol for runners and cyclists. Correlation analysis
did not reveal a significant relationship between pre-race
cortisol and testosterone (r = 0.114, p = 0.674) and between
post-race cortisol and testosterone (r = 20.399, p = 0.126).
DISCUSSION
The purpose of this study was to evaluate pre-race and post-race
responses of testosterone, cortisol, GH and IL-6 in endurance
trained cyclists and runners during the Susitna 100 ultraendurance race under extreme conditions. Although we have no
comparison conditions to determine the effects of such
117
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Original article
Table 1 Physical characteristics, pre-race and post-race body mass,
plasma volume and race time for runners and cyclists.
Table 2 Comparison of hormone responses with racing by bicycle
(cyclists; n = 6) and by foot (runners; n = 10)
Parameter
Runners (n = 10)
Cyclists (n = 6)
Exercise mode
Average age, years
Age, years (range)
Height, cm
Pre-race body mass, kg
Post-race body mass, kg
D Body mass, kg
% D Body mass
% D Plasma volume
Race duration, h
Shortest and longest race times, h
42 (7)
26 to 50
178 (5.0)
78.9 (7.1)
76.7 (7.4)
1.5 (1.5)
22.08 (2.13)
4.1 (8.7)
33.98 (6.12)
24.88 and 41.68
35 (9)
28 to 47
182 (5.0)
77.9 (10.6)
76.2 (8.3)
1.7 (2.8)
22.02 (3.11)
2.2 (11.1)
21.83 (6.27)
11.75 and 29.08
Cortisol, nmol/l
Runners
Cyclists
GH, mg/ml
Runners
Cyclists
IL-6, pg/ml
Runners
Cyclists
Testosterone, nmol/l
Runners
Cyclists
Data are presented as mean (SD) unless otherwise indicated.
independent variables as temperature, sleep loss and altitude,
these were all conditions related to the overall stress of the race,
and our data point to the gestalt of the stressful conditions
presented by the race. Overall, our data indicate that for both
runners and cyclists, pre-race to post-race levels of cortisol, GH
and IL-6 increased, whereas testosterone decreased.
Additionally, pre-race levels of circulating testosterone were
low (runners 12.32 (4.47) nmol/l: cyclists 13.81 (3.19) nmol/l)
compared with normal reference values (14 to 28 nmol/l).31 This
finding was consistent with previous research, which has shown
that men who have performed chronic endurance exercise for
many years have lower basal levels of free and total testosterone
compared with age-matched sedentary men.1
The cause of these suppressed resting testosterone levels
remains speculative. However, it is possible that the negative
feedback loop of hypothalamic–pituitary unit is unresponsive to
reduced levels of circulating testosterone. Pituitary LH regulates
testosterone production, but the present study did not measure
simultaneous circulating LH levels. However, Wheeler et al32
found that endurance-trained men with low basal testosterone
levels do not seem to have raised circulating LH levels. Thus, the
mechanisms of testosterone suppression remains uncertain, and
the pulsatile release of LH further challenges this understanding.
Furthermore, Hackney et al33 found that men with low basal
circulating testosterone showed a blunted response to an
exogenous gonadotropin releasing hormone (GnRH stimulus),
while testosterone production from the LH response seemed
normal. It could also be possible that the number of testicular
LH receptors on the Leydig cells may be reduced, resulting in
reduced testosterone production.1 LH receptor number can
possibly be reduced by persistent rises in circulating LH,
resulting in downregulation of receptor number; by the
presence of other hormones that can suppress testicular
function; or by the thermic effects of exercise training.1 34
Additionally, raised basal levels of follicle-stimulating hormone
(FSH) observed in endurance-trained athletes may provide
further evidence of hypogonadism compensation due to
intensive chronic training.15
Our data show no significant relationship between pre-race
levels of cortisol and testosterone. Furthermore, pre-race cortisol
levels of our endurance athletes were not above the normal
range.31 Similarly, other researchers have found resting levels of
cortisol in endurance-trained athletes to be similar to untrained
people.35 36 Nevertheless, some researchers have speculated that
raised cortisol levels, as a direct consequence of endurance
training37 and more specifically overtraining,38 is a plausible
mechanism to explain low basal testosterone. However, in our
investigation, it is unlikely that our athletes were overtrained,
118
Pre-race
Post-race
Effect size
142.09 (50.74)
245.83 (135.26)
452.21 (163.40)*
535.99 (232.22)*
0.37
0.32
0.12 (.23)
0.18 (.15)
3.21 (3.33)*
3.73 (1.30)*
0.87
0.84
2.42 (.68)
2.36 (.42)
12.25 (1.78)*
10.15 (3.28)*
0.76
0.74
12.32 (4.47)
13.81 (3.19)
6.96 (3.19)*
5.59 (3.74)*
0.78
0.72
GH, growth hormone; IL-6, interleukin-6.
*All post-race values are significantly (p,0.05) different from the corresponding prerace value.
Data are presented as mean (SD) unless otherwise indicated.
and the training of these athletes was not a significant source of
physical stress inducing raised resting cortisol levels. It has been
proposed that these stress hormones may be responsible for the
feedback disruption, as strong negative relationships have been
observed between testosterone and cortisol.39–41 Furthermore, it
should be noted that there was a large variation in pre-race
cortisol. The reason for this is possibly attributable to the
pulsatile nature of cortisol release.42 43 Moreover, cortisol release
is highly responsive to physiological stress, nutrition and
exercise status,44 45 sleep46 and environmental conditions,23 24
which may have posed varying levels of physiological stress
for individual athletes.
The race imposed a significant physical and metabolic stress, as
indicated by the hormonal responses. Post-race testosterone levels
significantly declined, whereas cortisol, GH and IL-6 significantly
increased relative to pre-race values. Several feasible mechanisms
may explain the decreased post-race levels of testosterone, where
either the rate of testosterone utilisation increased to exceed
production during the race to preserve protein tissue or the rate of
production decreased during the race because of inhibitory
mechanisms. At the anterior pituitary (central) level of the HPG
axis, the pulsatile release of LH may have decreased or become less
frequent because of competing mechanisms while GH production
was preferentially increased for immediate exercise effects to
provide energy. McColl et al11 showed that exercise induces a
Figure 1 Pre-race and post-race growth hormone and testosterone
responses for the cyclists. Dashed line between black triangles, mean
value; horizontal dashed line, normal values for men.
Br J Sports Med 2008;42:116–120. doi:10.1136/bjsm.2007.035535
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Original article
What is already known on this topic
c
c
The physiological stress of endurance exercise, both acute and
chronic, suppresses the hypothalamic–pituitary gonadal axis
in men.
Environmentally cold conditions present an additional stress to
humans in trying to maintain thermoneutral internal
temperatures, where hormones play an important role.
What this study adds
c
Figure 2 Pre-race and post-race growth hormone and testosterone
responses for the runners. Dashed line between black triangles, mean
value; horizontal dashed line, normal values for men.
general lowering of LH levels but does not inhibit LH pulsatile
release. Additionally, blood flow and substrate precursor availability (eg cholesterol, pregnenolone) to the testes may have
decreased,1 limiting the rate of testosterone production at the
peripheral level of the HPG axis. These plausible alterations in
blood flow in the testes may affect b-endorphin and nitric oxide
mechanisms related to testosterone secretion.47–49
Cortisol was possibly raised after the race to maintain plasma
glucose level, a response that is commonly observed in
endurance exercise.50 Cortisol has been shown to reduce
testosterone level when it is directly infused into men. The
mechanism for this effect is possibly due either to its direct
inhibition of testosterone production by the Leydig cells or to
feedback disruption of the HPG regulatory axis. However, our
data showed no significant correlations between levels of
cortisol and testosterone after the race. Several factors could
explain this null finding in hormonal responses, including large
variations among the athletes, the time course and/or the
c
c
Baseline hypogonadal levels of testosterone indicate a
suppression of the hypothalamus–pituitary–gonadal axis in
ultra-endurance athletes.
Reduced circulating testosterone and increased cortisol,
growth hormone and interleukin-6 levels in the ultra-endurance
event is indicative of the combined physiological and
environmental stresses on the ultra-endurance athletes before
and during the event.
Training and nutritional protocols need to be devised to obviate
such negative physiological homeostatic profiles, especially
before the event.
magnitude of individual stress responses. Similarly, Daly et al40
showed no significant negative relationships between cortisol
and free testosterone in endurance-trained men exercising to
exhaustion at 100% of their ventilatory threshold.
GH has been shown to facilitate both the glucose regulatory
and protein synthesising actions of cortisol, hence the corresponding increase. Furthermore, other researchers have noted
increased GH levels with prolonged running.51 Additionally, IL-6
has been shown to increase in response to exercise52 and low
skeletal muscle glycogen stores.53 IL-6 is released from active
Figure 3 Mean pre-race and post-race
levels of (A) testosterone, (B) cortisol, (C)
growth hormone, and (D) interleukin-6, for
runners and cyclists.
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skeletal muscle to mobilise extracellular substrate oxidation rate
(via enhanced lipolysis)54 and/or augment substrate delivery
during exercise.55 IL-6 release from the exercising muscle
possibly signals the liver to increase its glucose output to
preserve blood glucose levels during exercise,56 which plausibly
explains the increase seen in these athletes after the race.
In summary, these data provide specific hormonal information on athletes undergoing extreme physiological stress during
an actual competition. Data suggest possible suppression of the
HPG axis by an ultra-endurance race under such extreme
conditions and support the observation that endurance-trained
men show lower basal levels of testosterone compared with
normal healthy non-endurance-trained males.
28.
Competing interests: None.
37.
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Commentary
This is an excellent paper that evaluates the hormonal response
to an ultra-endurance event in frozen temperatures. Research on
endurance exercise in very low ambient temperatures is unique
and has been essentially ignored by the scientific community,
making this paper valuable to those both participating in these
events and to those designing training programmes. One of the
most distinctive aspects of this paper is the low correlation
between cortisol and testosterone both before and after races.
Lee E Brown, Cal State University, Fullerton, USA; [email protected]
Br J Sports Med 2008;42:116–120. doi:10.1136/bjsm.2007.035535
Downloaded from http://bjsm.bmj.com/ on May 16, 2016 - Published by group.bmj.com
Hormonal responses to a 160-km race across
frozen Alaska
W J Kraemer, M S Fragala, G Watson, J S Volek, M R Rubin, D N
French, C M Maresh, J L Vingren, D L Hatfield, B A Spiering, J Yu-Ho, S
L Hughes, H S Case, K J Stuempfle, D R Lehmann, S Bailey and D S
Evans
Br J Sports Med 2008 42: 116-120 originally published online July 17,
2007
doi: 10.1136/bjsm.2007.035535
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