Skiing across the Greenland icecap: divergent effects on limb muscle adaptations and substrate oxidation
1 Copenhagen Muscle Research Centre, National University Hospital,
Denmark
2 Department of Applied Physiology, Polish Academy of Science, Warsaw,
Poland
3 Department STAPS, University of Savoie, France
* Author for correspondence (e-mail: jhelge{at}cmrc.dk)
Accepted 10 January 2003
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Summary |
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Key words: triceps brachii, vastus lateralis, enzyme activity, fat mass, exercise, muscle, oxygen uptake
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Introduction |
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We have consistently shown that the diet composition during endurance
training markedly influences both substrate utilisation during exercise and
skeletal muscle adaptations observed after training
(Helge and Kiens, 1997;
Helge et al., 2001
). During
arm or leg exercise performed at the same relative load of
O2max, there is
a higher muscle glycogen utilisation and a higher lactate output during arm
compared with leg exercise (Ahlborg and
Jensen-Urstad, 1991
). However, it is not clear how prolonged,
whole body, low-intensity training will affect substrate oxidation during
submaximal arm or leg exercise. Furthermore, as diet was not controlled in the
study by Turner et al. (1997
)
and was only partially controlled (high carbohydrate in weeks 2 and 3) in the
study by Schantz et al.
(1983
), this may have
influenced the adaptive response in leg and arm muscle after the endurance
training period.
Crossing the Greenland icecap on cross-country skies pulling heavy sledges demands an extreme load on the human body, where both legs and upper body are engaged. Moreover, although the diet contained a dominance of carbohydrate (CHO), the reliance on lipid oxidation will be very high. The study of people performing the crossing offers a unique opportunity to test the hypothesis that the two factors, moderate but extensive daily exercise combined with a high total fat combustion, elicit an extreme adaptation of limb skeletal muscles, which in turn results in an elevated contribution of fat for energy during exercise. The aim of this study was to investigate the adaptive response in limb muscle and the substrate oxidation during submaximal arm or leg exercise after a cross-country skiing expedition over the Greenland icecap.
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Materials and methods |
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The subjects commenced the crossing from Kangerlussuag on the west coast of Greenland on 2 May 2001 and finished in Isortoq on the east coast on 12 June 2001. The subjects travelled for a total of 42 days. However, 5 days were spent resting in the tents due to harsh weather conditions. The total distance covered was approximately 650 km, and an altitude of 2500 m above sea level was reached. The peak altitude was reached after approximately 430 km and the skiing was, until this point, performed with `skins' under the skis. In this situation, the friction from the direction of the hairs (mohair or synthetic) on the skin mounted under the ski prevents the ski from sliding backwards. Furthermore, the forward motion of the ski is easier if the ski is slightly lifted during the forward motion. Each subject pulled a sledge weighing initially 120 kg. During the passage, the day temperature ranged between30°C to 0°C and some wind was experienced. On average, the subjects spent approximately 8-9 h day-1 on cross-country skies pulling the sledges. The subjects took turns leading the other members of the expedition, making snow tracks, with a new person taking the lead every 15 min. After each member had taken a turn at the front (approximately 60 min), breaks were taken. Due to the cold conditions, most breaks lasted less than 10 min and only the lunch break was slightly longer (approximately 15-25 min). The food consumed during the passage was pre-packed and carried by the subjects. The diet was a standard high CHO diet consisting of a breakfast, lunch and evening meal and a variety of snacks for consumption during the day. The nutrient composition expressed as a percentage of consumed energy was 9±1% protein, 31±1% fat and 60±1% CHO. During the first part of the passage expedition, the subjects were not able to consume their calculated daily ration. However, during the later part, food intake was increased and subjects were able to consume their full daily ration together with the food that was not consumed during the first part. Based on individual descriptions of mean daily dietary intake, it can be calculated that the mean daily energy consumption was 18.6±1.2 MJ. The consumed amount of CHO provides approximately 8.5±0.6 g CHO kg body mass-1.
Experimental protocol
On two consecutive days prior to departure and again five days after the
expedition, the subjects came to the laboratory, having fasted for 6-7 h, to
perform maximal and submaximal upper and lower limb exercise tests. The
subjects were asked to refrain from vigorous physical activity on the day
preceding the first testing session. After an initial rest period, a needle
biopsy was obtained with suction from the vastus lateralis muscle and from the
triceps brachii (lateral head). After this procedure, a catheter was inserted
into an antecubital vein for collection of venous blood during the exercise
tests. Throughout the exercise testing, the catheter was intermittently
flushed with sterile sodium chloride to maintain patency. Prior to exercise,
body mass (kg) and skin fold measurements (mm) were performed
(Durnin and Womersley, 1974).
After a 15 min rest period, a venous blood sample was obtained and exercise
initiated. On the first day, subjects performed lower limb bicycle ergometer
exercise (Monark 839E; Monark Exercise AB, Vansbro, Sweden) consisting of 10
min at 100 W followed by 10 min at 200 W. On the second day, subjects
completed upper limb modified arm cranking exercise involving 10 min at both
45 W and 100 W. The arm ergometer (Monark 884E; Monark Exercise AB) was
mounted on an aluminium frame and adjusted to the shoulder height of the
subjects. This exercise model requires utilisation of the muscles of the arms
and the upper body (Secher et al.,
1977
). On both days, after the submaximal exercise bouts, a
standard
O2max
test to exhaustion was performed, where the workload was progressively
increased by 40 W min-1 and 20 W min-1 in leg and arm
cycling, respectively. Blood samples were collected during the final 2.5 min
of each of the submaximal exercise loads and immediately after termination of
exercise. In addition, a blood sample was collected 3 min after termination of
the exercise test. Pulmonary oxygen uptake
(
O2) and carbon
dioxide excretions
(
CO2) at rest
and during exercise were measured by an automated on-line system (CPX; Medical
Graphics, Spiropharma, Denmark).
Analytical procedures
Blood was transferred into tubes containing 0.3 mol l-1 EDTA (10
µl ml-1 blood) and immediately centrifuged at 4°C for 10 min
at 23,000 g. A small fraction of the blood was transferred
into tubes containing EGTA, and this was later used for the insulin and
catecholamine determinations. The plasma was stored at -80°C until
analysis. Plasma glucose and lactate were analysed on an automatic analyser
(Cobas Fara, Roche, Basel, Switzerland). Plasma glycerol was analysed as
described by Wieland (1974),
and plasma fatty acid (FA) concentration was measured using a Wako NEFA-C test
kit (Wako Chemical, Neuss, Germany); both were determined on an automated
analyser (Cobas Fara, Roche, Basel, Switzerland). Insulin in venous plasma was
determined using a radioimmunoassay kit (Insulin RIA100; Pharmacia, Stockholm,
Sweden). Catecholamines in venous plasma were determined by a radioenzymatic
procedure (Christensen et al.,
1980
). Haemoglobin was determined on a HemoCue (HemoCue AB,
Ängelholm, Sweden).
The muscle tissue was frozen in liquid nitrogen within 10-15 s of sampling.
Before freezing, a section of the samples was cut off, mounted in embedding
medium and frozen in isopentane, cooled to its freezing point in liquid
nitrogen. Both parts of the biopsy were stored at -80°C until further
analysis. Before biochemical analysis, muscle biopsy samples were freeze-dried
and dissected free of connective tissue, visible fat and blood using a
stereomicroscope. Myosin heavy chain composition was analysed as described by
Andersen and Aagaard (2000).
Muscle capillary density was analysed, visualised and quantified as described
by Qu et al. (1997
). In the
serial transverse muscle sections, fibre types were stained for myofibrillar
ATPase as described by Brooke and Kaiser
(1970
). The fibre type
determined from the myosin heavy chain (MHC) composition was in agreement with
the fibre type distribution quantified by traditional histochemistry both
before and after the expedition (histochemical fibre type data are not
included).
The maximal activity of the enzymes ß-hydroxy-acyl-CoA-dehydrogenase
(HAD), citrate synthase (CS), phospho-fructokinase (PFK) and lactate
dehydrogenase (LDH) were determined fluorometrically according to Lowry and
Passonneau (1972).
Hormone-sensitive lipase activity (HSL) was assayed as described by Langfort
et al. (1998
). For the
determination of LDH isozymes, identified as LDH1, LDH2,
LDH3, LDH4 and LDH5, muscle homogenates were
prepared by centrifugation at 190 000 g for 90 min at 4°C,
and LDH activity was measured in the supernatant
(Brooks et al., 1999
). After
protein content determination with a bovine serum albumin (BSA) standard (DC
protein assay; BioRad, Hercules, CA, USA), 1.5 µg of protein was loaded
onto 1% agarose gels and separated for 45 min at 90 V using a Bio-Rad Sub-Cell
system. LDH isozymes were revealed colorimetrically with a commercial kit
(procedure no. 705-EP; Sigma Diagnostics, St Louis, MO, USA). Gels were fixed
in 5% acetic acid and scanned. Band densities were quantified by software
analysis with SigmaGel (SPSS Science Software GmbH, Munchen, Germany).
Calculations
Body density was determined from the skin fold measurements, and,
subsequently, body fat (%) was calculated from the body density according to
the method of Siri (1961). The
LDH isozyme results were expressed as a proportion of the H or M subunits
(H-LDH and M-LDH, respectively). H-LDH and M-LDH were estimated as follows
(Linossier et al., 1997
):
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The HOMA insulin resistance index, described originally by Matthews et al.
(1985) and modified recently
by Jenkins et al. (2000
), was
calculated according to the latter. In brief, fasting plasma insulin and
fasting plasma glucose values were used to calculate an index of insulin
resistance (HOMA-Rmod; Jenkins
et al., 2000
). There is a direct correlation between the insulin
resistance index and insulin resistance as measured by the euglycemic clamp
technique (Jenkins et al.,
2000
).
Statistics
Results are given as means ± S.E.M., if not otherwise stated. As the
number of subjects was so small, formal statistics are not applied to
discriminate changes due to the intervention. However, to underline the major
changes, we have added the general direction of change after the intervention
(for example, `three of three subjects' implies the same directional change in
all three subjects). In addition, Pearson correlation was applied to the
dataset (SigmaStat 2.0, SPSS Science Software, Erkrath, Germany, Germany).
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Results |
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Muscle citrate synthase activity was decreased (three of three subjects) in vastus lateralis but remained unchanged in triceps brachii after the passage (Table 2). The ß-hydroxyacyl-CoA-dehydrogenase activity was lower in two of three subjects in vastus lateralis after the passage, whereas no change was apparent in triceps brachii after the passage (Table 2). Hormone-sensitive lipase activity was not changed in either vastus lateralis or triceps brachii after the passage (Table 2). Phospho-fructo-kinase activity was decreased (three of three subjects) in both muscles after the passage (Table 2). The lactate dehydrogenase activity was not altered after the passage in either triceps brachii or vastus lateralis (Table 2). By contrast, the expression of muscle-type-specific LDH (M-LDH) was decreased (three of three subjects) in vastus lateralis after passage, whereas it remained unchanged in triceps brachii (Table 2). The M-LDH expression was approximately 80% higher in triceps brachii than in vastus lateralis (Table 2). When all sample points are included, i.e. arm and leg muscle, before and after the passage, a very strong correlation is shown between LDH activity and % M-LDH expression (rPearson=0.84, P<0.001, N=3).
|
During the initial exercise test, the
O2 during arm
exercise was 1.1±0.1 l min-1 and 2.4±0.1 l
min-1 at 45 W and 100 W, respectively, and during leg exercise was
1.6±0.1 l min-1 and 2.7±0.11 min-1 at 100
W and 200 W, respectively. When the subjects returned and performed the
submaximal exercise at the same absolute workload, the
O2 was similar
to that measured in the initial test. The relative exercise intensity (%
O2max) remained
unchanged during the pre- and post-tests (35±2% and 43±3% at the
lower submaximal work loads in arm and leg, respectively; 73±3% and
72±2% at the higher submaximal work loads in arm and leg,
respectively). After the expedition, the respiratory exchange ratio (RER) was
lower during arm exercise at both the lower (four of four subjects) and the
higher (three of four subjects) submaximal workload compared with the initial
test (Fig. 2A). By contrast,
the RER was higher during leg exercise at the lower (four of four subjects)
and the higher (three of four subjects) submaximal workload
(Fig. 2B). During the initial
test, the expiratory ventilation
(
E) during arm exercise was
29±21 min-1 and 66±61 min-1 at 45 W and
100 W, respectively, and during leg exercise was 43±31 min-1
and 72±41 min-1 at 100 W and 200 W, respectively. When the
subjects returned and performed the submaximal exercise at the same absolute
workload, the
E was similar
to that observed in the initial test. The ratio between
E and
O2
(
E/
O2)
during arm exercise was similar before and after crossing: 27±21 air 1
oxygen-1 and 32±41 air 1 oxygen-1 at 45 W and 100
W, respectively. By contrast, the
E/
O2
during leg exercise was increased (four of four subjects) from 22±21
air 1 oxygen-1 and 24±21 air 1 oxygen-1 before
the crossing to 27±21 air 1 oxygen-1 and 27±11 air 1
oxygen-1 after the crossing at 100 W and 200 W, respectively.
|
Prior to departure, haemoglobin concentrations were 9.3±0.3 mmol l-1, and, although an altitude of 2500 m was reached during the crossing, no increase in haemoglobin concentration was observed after returning (9.4±0.4 mmol l-1). Prior to exercise, post-absorptive plasma glucose concentration was similar on the four experimental days (Fig. 4A). However, plasma insulin was slightly higher (three of four subjects) after the passage (Fig. 3A), as was a calculated HOMA insulin resistance index (three of three subjects; Fig. 3B). Plasma glucose concentration was unchanged across the different exercise intensities or in recovery (Fig. 4A). Plasma lactate concentration at rest was similar on the four experimental days (Fig. 4B). As expected, plasma lactate concentration increased (four of four subjects) when exercise intensity was increased (Fig. 4B). During arm exercise, both at submaximal and maximal workloads, plasma lactate concentration was slightly higher (four of four subjects) than when leg exercise was performed at comparable relative workloads (Fig. 4B). Prior to departure for Greenland, plasma fatty acid (FA) concentration at rest was similar on the two experimental days (Fig. 4C). Interestingly, plasma FA concentration at rest was markedly decreased (four of four subjects) on both experimental days when the subjects returned from Greenland. During submaximal exercise in the pre-testing, both during arm and leg exercise, plasma FA was lower (four of four subjects) as exercise intensity increased. By contrast, there was no effect of exercise intensity, in either arm or leg exercise, on the plasma FA after the passage (Fig. 4C). Prior to exercise, fasting glycerol concentration was similar on the four experimental days (Fig. 4D). In the two arm exercise tests, before and after passage, plasma glycerol concentration increased (four of four subjects) similarly as exercise intensity was increased. By contrast, plasma glycerol concentration was lower (four of four subjects) at the different exercise intensities after the passage when leg exercise was performed (Fig. 4D).
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Prior to exercise, venous adrenaline and noradrenaline concentrations were similar on the two experimental days: 2.5±0.4 nmol l-1 adrenaline and 0.5±0.15 nmol l-1 noradrenaline. At the different exercise intensities at the pre-tests, both during arm and leg exercise, the venous adrenaline and noradrenaline concentrations increased (four of four subjects) similarly and to the same level (40±8 nmol l-1 and 8.6±2.9 nmol l-1 at max, respectively) as exercise intensity increased. After the passage, the venous adrenaline and noradrenaline concentrations increased (four of four subjects) as exercise intensity was increased and, compared with the pre-passage values, the values after passage were 25±3% lower overall.
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Discussion |
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It is well known that, after a period of endurance training, substrate
utilisation during exercise at a given absolute workload is altered towards a
larger combustion of lipids at the expense of carbohydrates
(Henriksson, 1977;
Gollnick, 1985
). This
alteration in substrate utilisation is thought to occur due to increases in
local muscle mitochondrial volume, capillarisation and oxidative enzyme
activity, as well as in whole body oxygen uptake capacity
(Holloszy and Coyle, 1984
;
Saltin and Gollnick, 1983
).
Furthermore, there is evidence that manipulation of dietary intake, primarily
the carbohydrate-to-fat ratio, during adaptation to endurance training can
also markedly alter substrate utilisation during submaximal exercise after
training (Helge et al., 1996
,
2001
). By contrast, the shift
towards a higher fat utilisation during submaximal arm exercise occurred
despite a high carbohydrate diet in combination with no change in muscle
oxidative enzyme activity and only a minor increase in capillarisation.
Apparently, this adaptation is specific to the triceps brachii muscle, since
the higher carbohydrate oxidation observed during submaximal leg exercise in
the present study is consistent with the decreased oxidative enzyme activity
in vastus lateralis and the effect of a high carbohydrate intake on substrate
utilisation. The observation of a difference in the adaptation pattern between
arm and leg muscles is consistent with the findings of Schantz et al.
(1983
) and Turner et al.
(1997
) after whole body
training or training of both arms and legs, respectively. However, these
studies did not report whether the induced adaptation influenced the limb
substrate utilisation during exercise. In the present study, we investigated
the triceps brachii and the vastus lateralis, as we considered both of these
muscles to be of prime importance for cross-country skiing, particularly as
this also included pulling a heavy sledge and using skins though the majority
of the crossing. However, although we consider it unlikely, we cannot exclude
the possibility that other upper and/or lower body muscles may exhibit an
adaptation pattern that is different to that observed in triceps brachii and
vastus lateralis.
In the present study, the crossing resulted in a loss of 5.7 kg of body
mass, the majority of which was body fat, indicating the presence of an
overall energy deficit (approximately 5 MJ day-1) during the
crossing. It is not clear how this energy deficit affected substrate
utilisation during exercise and rest but, inevitably, it must have stimulated
utilisation of body fat reserves. As reported by Stroud et al.
(1997), two explorers crossed
Antarctica, under very strenuous conditions, on cross-country skies pulling
very heavy sledges and consuming a high fat diet (57% fat, 35% carbohydrate).
Based on the doubly labelled water technique and calculated energy balance
data, it can be estimated that their average daily energy deficit ranged
between 3 MJ and 27 MJ. Over the 95 days, the two subjects lost approximately
25% of their body mass and, when the crossing was stopped on health grounds,
there was almost no body fat present
(Stroud et al., 1997
). No
attempt was made to quantify exercise substrate utilisation during or after
the Antarctic crossing. However, it is clear that energy for the exercise
performed must, to a large extent, have come from fat. In both subjects,
muscle oxidative capacity in vastus lateralis and maximal whole body oxygen
uptake was significantly declined after the crossing
(Stroud et al., 1997
),
indicating that skeletal muscle under strenuous conditions and severe energy
deficit has a large capacity to metabolise fat. Further support for this comes
from a study of migrating Great Knots (Calidris tenuirostris), which
were studied before and after a 5400 km migration and compared with a group of
captured birds that were fasted for a fortnight
(Battley et al., 2001
). Using
this model, it was demonstrated that migrating birds were able, to a large
extent, to sustain flight primarily using fat as substrate and, furthermore,
to keep lean tissue loss to a minimum
(Battley et al., 2001
). In the
present study, the fibre type area of both type I and type II fibres tended to
be increased in the triceps brachii after the crossing, which suggests that
extra muscle protein was added despite the energy deficit. Overall, this
implies that there is some similarity between the adaptation patterns in arm
muscle after prolonged, low-intensity exercise and the adaptation pattern
observed in migrating bird flight muscle.
Due to the design and conditions of the present study, we could not assess
changes in muscle substrate stores immediately before or after the crossing.
However, one possible explanation for the high fat oxidation during arm
exercise is that intramuscular triacylglycerol stores become located, to a
higher degree, around the mitochondria
(Vock et al., 1996), which
makes the FA, recruited via breakdown of triacylglycerol, more
accessible for oxidation. Unfortunately, due to large inter-individual
variations, our measurement of hormone-sensitive lipase does not allow us to
expand on this. However, the finding of an unchanged venous glycerol response
at the different arm exercise intensities, contrasting to the significantly
decreased glycerol response during leg exercise, gives some support to
utilisation of intramuscular triacylglycerol, particularly as venous plasma FA
concentrations were very low throughout the different exercise
intensities.
Interestingly, we observed an increased plasma insulin concentration at
rest and an increased insulin resistance after the subjects had completed the
expedition. This is a noteworthy observation considering the amount of
physical activity that these subjects endured during the crossing. However, a
large part of the carbohydrates consumed during the crossing were simple
sugars (approximately 50-55%), which in several studies, both epidemiological
(Liu and Manson, 2001) and
interventional (Jeppesen et al.,
1997
; McLaughlin et al.,
2000
), have been linked to an adverse outcome in relation to
insulin resistance. Furthermore, there was, in fact, a slight decrease in lean
body mass after the passage, which is consistent with the observation of an
increased insulin resistance. Thus, the finding of an increased insulin
resistance index despite the arduous physical stress endured emphasizes the
need to consider both diet intake and physical activity in order to combat
insulin resistance.
In conclusion, a major finding in the present study is the marked increase in fat oxidation during submaximal arm exercise after a 42-day cross-country skiing expedition involving prolonged, low-intensity, whole body endurance training. This occurred despite only a minor increase in capillarisation and no change in oxidative capacity in triceps brachii muscle after training. The marked increase in fat oxidation during arm exercise, occurring despite a high carbohydrate intake, and an increase in muscle fibre type area do resemble the dramatic shift in fuel utilisation seen during migration in birds. Thus, with due respect to the limited number of subjects, we suggest that our current understanding of the effect of prolonged, low-intensity, whole body training on the arm muscle adaptation pattern needs reconsideration.
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Acknowledgments |
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