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Received: 2 September 2022    Revised: 19 October 2022    Accepted: 19 October 2022

DOI: 10.1111/sms.14268

SPECIAL ISSUE ARTICLE

High or hot—­Perspectives on altitude camps and heat-­


acclimation training as preparation for prolonged stage
races

Lars Nybo1   | Bent Rønnestad2   | Carsten Lundby2

1
Department of Nutrition, Exercise
and Sport, University of Copenhagen, Abstract
Copenhagen, Denmark Adaptation to heat stress and hypoxia are relevant for athletes participating in
2
Inland Norway University of Applied Tour de France or similar cycling races taking place during the summertime in
Sciences, Lillehammer, Norway
landscapes with varying altitude. Both to minimize detrimental performance ef-
Correspondence fects associated with arterial desaturation occurring at moderate altitudes in elite
Lars Nybo, Universitetsparken 13, athletes, respectively, reduce the risk of hyperthermia on hot days, but also as a
second floor, DK-­2100 Copenhagen Ø,
Denmark. pre-­competition acclimatization strategy to boost blood volume in already highly
Email: nybo@nexs.ku.dk adapted athletes. The hematological adaptations require weeks of exposure to
manifest, but are attractive as an augmented hemoglobin mass may improve ar-
terial oxygen delivery and hence benefit prolonged performances. Altitude train-
ing camps have in this context a long history in exercise physiology and are still
common practice in elite cycling. However, heat-­acclimation training provides
an attractive alternative for some athletes either as a stand-­alone approach or in
combination with altitude. The present paper provides an update and practical
perspectives on the potential to utilize hypoxia and heat exposure to optimize
hematological adaptations. Furthermore, we will consider temporal aspects both
in terms of onset and decay of the adaptations relevant for improved thermoreg-
ulatory capacity and respiratory adaptations to abate arterial desaturation dur-
ing altitude exposure. From focus on involved physiological mechanisms, time
course, and responsiveness in elite athletes, we will provide guidance based on
our experience from practical implementation in cyclists preparing for prolonged
stage races such as the Tour de France.

KEYWORDS
altitude, acclimatization, cycling, heat, performance, training

1  |  I N T RO DU CT ION “acclimation training” or natural acclimatization to ei-


ther hypoxia induced via altitude training camps or ad-
The present perspective will focus on the potential aptation to hyperthermia via exposure to environmental
performance benefits derived from pre-­ competition heat stress. Acclimatization here defined as the integrated
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any
medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2022 The Authors. Scandinavian Journal of Medicine & Science In Sports published by John Wiley & Sons Ltd.

Scand J Med Sci Sports. 2022;00:1–10.  wileyonlinelibrary.com/journal/sms  |  1


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2       NYBO et al.

adaptation occurring during natural exposure to the envi- increased thermoregulatory capacity associated with im-
ronment, while “acclimation training” is considered as ex- proved sweat gland function (the sudomotor response),
posure that may induce similar physiological adaptation while for hypoxia, we will focus on the increased respira-
via specific exposure to heat stress or hypoxia, typically su- tory drive that may minimize arterial desaturation for a
perimposed in artificial settings (e.g., climatic chambers, given environmental oxygen pressure.
training with increased isolation/clothing or by breath- Elite endurance exercise performances are undoubt-
ing air with a reduced oxygen fraction). We will consider edly complex in nature involving a multitude of facets and
physiological aspects related to the two environmental with several physiological factors still to be elucidated.
stressors and how associated adaptations may benefit per- Nonetheless, the importance of a highly developed car-
formance in prolonged cycling stage races such as Tour de diovascular system that allows for high aerobic energy
France, Giro di Italia and Vuelta a España. Similar to sev- turnover as influenced arterial oxygen delivery (product
eral other stage races or single day competitions, the route of maximal cardiac output and arterial oxygen content)
in the 3  week grand tours typically implies that athletes and skeletal muscle efficiency has been highlighted for
are exposed to altitudes varying from sea level to moun- decades. Of these, arterial oxygen delivery and the asso-
tain passages or stage finishes 2000 m above sea level and ciated superior maximal oxygen uptake (V̇o2max) is largely
riders will furthermore be challenged by thermal stress on ensured by the interplay of a highly adapted myocardium
days with profound heat stress. It will, therefore, be rele- allowing for enhanced diastolic filling, a high Hb-­mass
vant to consider pre-­event acclimatization both as a strat- and the skeletal muscle capability to extract and utilize
egy to minimize the marked fatigue that occurs with acute the majority of the delivered oxygen.5 Of particular inter-
exposure to heat or altitude and the potential “transfer est and importance for the present review, enhancing Hb-­
effect”—­that is the hematological adaptations that with mass is very attractive as it may both elevate the oxygen
sufficient stress (time and intensity-­wise) may increase carrying capacity per liter blood and promote the pump-
the athlete's hemoglobin mass (Hb-­mass) and potentially ing capacity of the heart, secondary to the Frank-­Starling
improve aerobic performance. In addition to considering mechanism.6
if the stress is adequate (altitude/level of hypoxia or hy-
perthermia) and time course required to induce acclima-
tion, it is also relevant to consider the decay and ability 3  |   HEMATOLOGIC AL
to maintain the achieved adaptation. Thus, for prolonged ADAPTATIONS DURING ALTIT U D E
stage races the first mountains, decisive stages or days EX POSURE
with heat stress may not take place in the immediate pe-
riod after acclimatizing, but mainly be relevant during the It has been recognized for more than a century, that the
second or third week of racing. In opposition to single day blood hemoglobin concentration [Hb] increases rapidly
competitions, this may complicate the timing of acclima- during exposure to high altitude and returns to baseline
tization and how much a pre-­competition acclimation (pre exposure) levels during the first weeks upon return
camp benefits performance in the later stages, when the to sea level. This hematological response to altitude re-
environmental heat or altitude exposure is most relevant. lates to hypoxia-­induced erythropoietin (EPO) secretion
from the kidneys and the associated potential to stimulate
erythropoiesis has attracted attention from cycling teams
2   |   H E M ATOLOG ICAL AN D “NON-­ and coaches as well as the classical exercise physiology
H E M ATO LO GICAL” ADAPTAT IO NS studies focused on utilizing “altitude training camps”
as an approach to improve endurance performances.7,8
Acute exposure as well as the subsequent adaptation However, elevated [Hb] is not necessarily indicative of
to both hypoxia and heat stress includes a plethora of increased Hb-­mass as altitude exposure already within
physiological responses and for comprehensive over- the first hours upon ascent is associated with a diuretic
view of mechanisms involved, we refer to recent reviews response that reduces the plasma volume and lower the
dedicated to provide insight in mechanisms involved in total blood volume1. Although, the increased hematocrit
acclimatization to hypoxia/altitude1,2 and for heat/hyper- and higher [Hb] increase the arterial oxygen carrying ca-
thermia.3,4 For brevity, we will in this perspective paper pacity, it will not benefit arterial oxygen delivery as it oc-
make a coarser classification and divide into attention on curs on the expense of a reduced maximal cardiac output.9
the hematological responses (mainly focused on changes It is, therefore, important to emphasize that [Hb] or hema-
in Hb-­mass, total blood and plasma volume), respectively, tocrit measures are insufficient to track or verify effects
“non-­hematological” adaptations. For heat acclimatiza- of an altitude training camp in terms of boosting blood
tion, the latter will mainly involve considerations on the volume. Rather, we recommend assessment of the total
NYBO et al.    |
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Hb-­mass, for example, with CO-­breathing or other appro- of exposure, a reduction in the total circulating blood vol-
priate methodologies10 and such measures have revealed ume is commonly observed at high altitude.7,9 Although,
that at least 3 weeks exposure is required to assure that the hematological responses to altitude exposure has been
the elevated EPO and enhanced erythropoiesis translate investigated for decades, its regulation remains to be com-
into significant higher Hb-­mass.11,12 In addition to suffi- pletely understood. It is clear that many mechanisms are
cient duration, altitude acclimatization also depends on involved, but the complexity of their interplay is not well
sufficient intensity of the stimuli (level of hypoxia) and described. This may both relate to difficulties in complet-
consistency of the exposure (hours per day). While “live ing well-­controlled comprehensive experiments and to di-
high—­train low” or acclimation via accommodation in vergent individual responses that remains to be revealed.
hypoxic chambers for some athletes may be an attractive In this review, we present our understanding of the kinet-
alternative and may allow for higher power output dur- ics, the mechanisms and in particular the physiological
ing training compared to “live and train high”, it may not (performance) relevance of the hypoxia-­induced reduc-
be recommended as it increases the risk for insufficient tion in PV, respectively, and the expansion in RCV.7
hourly exposure per day. For example, 4 weeks exposure From a practical point of view, residing for 3 weeks
to hypoxia equivalent to 2160 m above sea level for 17 h/ (or longer) in ~2500 m above sea level, staying and com-
day or 4 weeks at 3000 m for 16 h/day did not translate into pleting most training session at this altitude may fulfill
consistent elevation of Hb-­mass in RCT-­controlled stud- the exposure criteria in terms of “intensity” (the level
ies.13,14 In contrast, continuous exposure to 3450 m, which of hypoxia), duration and consistency of exposure. The
is higher than most coaches and athletes practice (but as daily training routes may naturally take riders to lower
discussed below, worthy of consideration) are associated altitudes for briefer periods without compromising the
with systematic elevations in Hb-­mass in recreationally abovementioned importance of consistent exposure.
active participants.11,15 The risk of “loosing training in- Going higher or staying longer either as permanent res-
tensity” as reflected in lower power output during train- idence or as practiced by mountaineers with intermittent
ing at altitude has been considered as an argument for -­shorter exposures (from one to few hours) to higher al-
“live-­high train-­low”.16 However, recent evidence from titudes on top of the basecamp residence—­would from
training intervention studies with superimposed hypoxia a physiological point of view provide a superior stimuli
suggest that although power output (in particular dur- and given the knowledge that a short intense/initial drop
ing intense aerobic intervals) will be lower at altitude, in arterial oxygen pressure will stimulate EPO, it could
the training will still provide a physiological stimuli suf- be used as strategy to further enhance the erythropoietic
ficient or as discussed below perhaps superior in terms of response. Indeed, in national team XC-­ski members the
stimulating some peripheral/muscular adaptations.17,18 live high—­train even-­higher approach has been shown
In terms of optimizing the hematological adaptation the to facilitate Hb-­mass expansion; currently only with ev-
“live high and train high-­approach” is, therefore, recom- idence from a one-­armed study design without control
mended. However, in terms of achieving higher power group,19 but the approach awaiting further scientific vali-
output and hence broader muscle fiber activation in some dation and it should also be realized that such “burst” in
training session, it may be considered to include short EPO when residing at sea level have not translated into
repeated exercise intervals (30/15 s intervals or similar) performance gains.7 If athletes are compelled to reside at
to allow for race pace relevant power output. This could lower altitudes for better training opportunities or ease of
especially be relevant for athletes such as track and field logistics, it could be considered to apply the “mountain-
distance runners, where a lower intensity could imply eering approach” by superimposing night time hypoxia
a marked change in the movement pattern and biome- (e.g., sleeping in hypoxic tents or chambers) aiming at fa-
chanical load. Humans ascending to high altitude experi- cilitating worthwhile adaptations. Here it is important to
ence an immediate reduction in arterial oxyhemoglobin note that hypoxic generators do not monitor barometric
saturation and consequently lower arterial O2 content and pressure and that a given reduction in the inspired O2 per-
reduced V̇o2max. If the exposure to altitude is extended, centage has larger effect when used at altitude compared
the reduction in V̇o2max is partly counteracted by an in- to sea level.
crease in arterial hemoglobin concentration. Initially, this In addition to sufficient time for altitude acclimati-
hemoconcentration is exclusively related to a reduction in zation to translate into elevated Hb-­mass, it is also very
plasma volume (PV), whereas after several weeks a pro- relevant to consider the time course for the decay upon
gressive expansion in total red blood cell volume (RCV) return to sea level. Observations, both from a one-­year ex-
contributes, although often to a modest extent. Since the posure study associated with a marked elevation in Hb-­
decrease in PV is more rapid and usually more pronounced mass (18% on average; Lundby et al. unpublished data)
than the expansion in RCV, at least during the first weeks and from the abovementioned 3–­4  week acclimatization
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studies,11,15 which increased Hb-­mass by 3%–­5%, signifies prepare for the altitude exposure taking place during the
that half of gained Hb-­mass is gone already 7 days upon second or third week of a grand tour.
return to normoxia and completely returned to baseline To summarize the above, both hematological and non-­
14 days after the altitude exposure.11,15 Thus, it is very im- hematological adaptations associated with high altitude
portant to stress that an altitude training camp should be exposure may develop following weeks of such contin-
completed in close proximity to the competitive period. uous exposure. It should be emphasized that at least he-
Altitude camps conducted in the winter or pre-­season are matological adaptations are only short lived upon return
in contrast unlikely to have any direct effects on perfor- to sea level and that altitude training camps should be
mance several months later unless something is done to planned accordingly.
prevent the decay.

5  |   HEAT ACC LIMATIZATION—­


4   |   N O N -­H E MATOLOG ICAL THE “ NON-­H EMATOLOGICAL”
A DA P TAT I ON TO HY POXIA ADAPTATIONS

Besides facilitating erythropoiesis, hypoxia may also stim- Heat acclimatization or acclimation protocols may be
ulate mitochondrial biogenesis as indicated by a 11.5% categorized into short (≤7 days/exposures), medium (8–­
increase in volume density of intermyofibrillar mitochon- 14 exposures) and long-­term (with more than 15 days
dria following 4 weeks at 3450 m in non-­athlete partici- of exposure)27 with the majority of studies and in par-
pants.20 It is often speculated that such adaptation may ticular experiments with elite athletes focused on the
benefit V̇o2max, but since the capacity for mitochondrial adaptations occurring during the first 1–­ 2 weeks. For
respiration is reported to vastly surpasses the ability of endurance-­trained athletes (adapting faster to heat than
O2 supply to the exercising skeletal muscle21 this is prob- untrained participants; see3,4 for overview) this period
ably of minor importance for athletic performance at least of time is sufficient to increase the maximal sweat rate,
in terms of increasing aerobic power. Improved electron lower the resting core temperature as well as the thresh-
transport efficiency, but reduced skeletal muscle mito- old for onset of sweating.28 Adaptations we consider as
chondria enzyme concentrations have been reported fol- three of the main “non-­hematological factors” of impor-
lowing both short (~2 weeks) and longer (4 weeks) altitude tance for increasing the thermoregulatory capacity and
exposure,22,23 but overall it appears that the respiratory allowing for increased exercise capacity in setting where
chain function remain unaltered22,23 and the potential per- the environmental heat stress is high and the ability to
formance consequences of these mitochondrial changes dissipate heat may limit exercise performance (i.e., ther-
remain unclear. mal balance rather than the athletes aerobic capacity be-
While altitude training camps often focus on improving comes limiting). As an example of relevance for cycling
performance upon return to lower altitudes (normoxia), it and the very fast onset of sudomotor adaptations occur-
is also relevant to consider that acclimatization is highly ring in athletes, we followed the time course of physi-
relevant for minimizing performance deterioration during ological and performance adaptations to heat exposure
races at altitude. Especially for highly trained athletes sus- during a two-­week intervention study (training camp
ceptibly to exercise-­induced arterial hypoxemia as it may with acute transfer from cold to heat).29,30 Acute expo-
impact performance already at low to moderate altitudes.24 sure provoked a 16% drop in power output (TT on first
The benefits from acclimatization are in this context faster day in the 36°C environment) compared to performance
than for the hematological responses as indicated by 3% in cool settings, but following acclimatization this was
increase in V̇o2max already following 1  week of acclima- reduced to less than 2% and no difference in time to
tization to 2350 m altitude and 7.5% after 2 weeks when complete the 43 km time trial used as the performance
V̇o2max in the trained athletes was tested at that altitude measure in that study (lower air density and hence resist-
and compared to the decline during acute exposure.25 ance fully compensated for the slight reduction in power
These early improvements are likely a consequence of a output).29 Indicators of sudomotor adaptation was ob-
lower degree of arterial desaturation with acclimatiza- served after only 2 days of exposure and sweat rate both
tion,26 although saturation for a given oxygen pressure re- in a standardized heat-­exposure test and during peak
mains below that of high altitude natives. The later could performance significantly increased on day 5–­6 with no
explain why athletes born and raised at high altitude may further increase during the second week. This signifies
have more permanent physiological advantage in this en- a very fast (completed in less than 1 week) improvement
vironment. Also, native lowlanders may experience a fast in sweat gland function and associated increase in cool-
decay of this adaptation, which complicates the ability to ing capacity, but also how vulnerable the non-­prepared/
NYBO et al.   
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unacclimatized rider will be during the first days of a an increase in Hb-­mass. As illustrated by Figure 1 derived
heat-­wave compared to a competitor that have acclima- from a point-­counter point discussion in 2016 in Journal
tized ahead of the race. of Physiology36,37 both 10 days heat-­acclimation32,38 and
Thermal adaptation requires a series of sufficient ther- 14 days with natural heat acclimatization30 can induce a
mal impulses, which for heat acclimation in practice may marked increase in plasma volume, but the PV-­expansion
be achieved by a variety of different approaches as long as in those studies was not associated with a change in peak
the heat stress exceed the required threshold and facili- power or time trial performance in trained cyclists. In op-
tates adaptation.4,27 The abovementioned study by Karlsen position to our opponents in the abovementioned point-­
et al.29 exemplifying natural acclimatization achieved via counter point discussion30 and their acclimation study,33
ecological exposure was completed as an intervention we found no evidence for short to medium duration heat
study where the HEAT-­group for 2 week transferred from acclimatization to translate into improved performance
habitual cool training environment to training in dry heat in cooler settings, although the athletes had massive im-
(~35°C with 2–­4  h exposure per day). However, similar provements in exercise performance tested in the heat.
physiological adaptations may be induced with shorter The evidence for “cool performance” transfer effects de-
(~1  h/day) training in climatic chambers31,32 or training rived from plasma volume expansion or other acclimation
with increased clothing33,34 (so-­called sweat suit training effects achieved via short-­medium duration acclimatiza-
that hampers heat-­dissipation to provoke hyperthermia). tion protocols are in our opinion still weak (see36,37 for
From a practical point of view and discussed below the discussion or this paper27 for meta-­analysis). The point-­
later may be attractive for some athletes as it may induce counter point discussion did, however, prompt us to com-
physiological adaptations comparable to natural expo- plete a series of prolonged heat-­acclimation studies31,33–­35
sure and allow the athlete to complete the remaining of with durations of 5 weeks or more to test the idea that
the weekly training in cooler conditions. As discussed in allowing sufficient time for adaptation, heat-­acclimation
recent consensus recommendation3 the natural exposure and the associated plasma volume expansion would trans-
may be preferred to allow athlete to familiarize with the late into an increased RBC-­volume.
perception of the environment. For cyclists, for example, Utilizing the prolonged heat-­ acclimation approach,
test how much the specific settings (integrated effects of accomplished either as part of the training (~1 h per day
air temperature, humidity, solar radiation and wind) af- and at least five times per week) completed in hot cli-
fects performance and hence may influence their pacing matic chambers31,34 or via training with superimposed
strategy and hydration requirement. This may be more heat stress with increased clothing insulation,33 we ob-
important in the early phases of a career, while it for expe- serve systematic increases in Hb-­mass both in elite in-
rienced athletes that may be less of an issue and they will ternational and national level competitive cyclists (see
benefit from the physiological preparation independent of Figure  2 for individual Hb-­mass gains across the range
the acclimatization/acclimation mode. of trained to highly trained athletes in the studies). On
average the 5 week heat-­training interventions, we have
completed elicit a ~3% effect (30 g gain) on total Hb-­mass,
6   |   H E M ATOLOG ICAL which is significantly different from matched controls
A DA P TAT I ON S TO PROLON G E D and translate into elevated peak peak-­powerpower during
H E AT ACC L IM AT ION incremental testing (delta gain of 18 watt in heat-­exposed
groups compared to 6 watt in control; p < 0.05 both for the
While short to medium duration acclimation protocols Hb-­mass and peak power response). We also observe in-
are adequate for athletes to improve/maximize sweat creased average power output during time trials (pre-­post
gland function and increase the resilience to environ- increase of 20 watt for medium duration [15–­30 min] time
mental heat stress, the duration required for completion trials completed in the lab on stationary bikes), but for
of the hematological adaptations makes long-­term heat-­ this performance measure with no difference compared
acclimation relevant. Although, acting via quite differ- to the control groups (as they also improve their time
ent mechanisms than hypoxic exposure35 the two modes trial power output). The later exemplifying the complex-
are similar in terms of requiring sufficient time (weeks ity of completing interventions studies with competitive
of exposure) to allow for red blood cell formation. Short-­ cyclists, but also that the heat-­interventions (substitut-
duration heat acclimatization may markedly increase the ing ~5 h of the weekly training volume with training in
plasma volume (also in highly trained athletes), but pro- heat with matched rating of perceived exertion, but lower
longed heat-­acclimation protocols with several weeks of power output) has the potential to improve all measures
exposure are required before the plasma volume expan- of performance in the heat, induce a meaningful increase
sion (plateauing within the first week) is accompanied by in Hb-­mass (even in highly trained athlete) and with no
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6       NYBO et al.

F I G U R E 1   Changes in physiological performance capacity evaluated in cool conditions (triangles representing average power
output during time trials [TT] and squares representing peak aerobic power during incremental exercise testing) versus the percentage
change in plasma volume following acute plasma volume expansion (filled symbols; albumin infusion) or 2 weeks of natural outdoor heat
acclimatization (open symbols). The symbols represent individual values from Karlsen et al.30 and Keiser et al.32 with the delta changes
calculated as the percentage increase from control. Both for peak power in incremental testing and for TT performance in cool setting there
was no effect following the medium-­range (10–­14 days) heat acclimatization or acclimation protocols despite marked elevation in plasma
volume.37

negative consequences for simultaneous improvements and matched control groups, the scientific research in-
of TT performance in cool settings. Also, it appears that cluding the prolonged heat-­acclimation studies that we
the loss of adaptation (return of Hb-­mass to baseline) have completed are usually completed during the pre-­or
can be prevented for a prolonged period via relatively few off-­season. However, from case observations including
(3 weekly) maintenance training sessions,39 which may Hb-­mass evaluations from professional cyclists,40 it is our
make the heat-­training approach more attractive than experience that both heat-­training and altitude camps
altitude training, where the decay is fast and difficult to can induce similar responses in cyclists during the com-
prevent. petitive season—­if the interventions comply with previ-
ously mentioned guidelines on duration and intensity.
The ability to complete controlled in-­season studies is dif-
7   |   P R ACT ICAL ficult (if not impossible) and evaluation of performance
RECO M M E NDAT ION S AN D effects are not straight forward to use for systematic
P E RS P ECT I VE S FOR FU RT HE R evaluation as changes in race schedule, mental stressors,
I M P ROV E M EN T S sickness or fatigue following races may interfere with the
performance effects. For practical in-­season purposes we,
The above studies serve as proof of principle that the therefore, advocate for monitoring the physiological fac-
interventions can induce physiological meaningful tors of relevance (e.g., sweat rate, respiratory-­or blood
improvements in highly trained cyclists and that su- lactate-­responses to a standard exercise bout and Hb-­
perimposed environmental stress in practice can be im- mass changes) either to supplement or substitute for per-
plemented in elite athletes training program. To allow formance testing as tracer of adaptation. This approach
for a very systematic approach with “clean interventions” may be suitable both in terms of monitoring the onset and
NYBO et al.   |
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F I G U R E 2   Delta changes (post–­pre) Heated room


in total Hb-­mass following prolonged 160 Sweat Suit
heat-­acclimation studies (5 weeks or 140
more) completes in heated room (climatic
120

Delta change in Hb-mass (g)


chambers—­open symbols) or training
in “sweat suit” (closed symbols) plotted 100
against the participants initial maximal
aerobic power (peak oxygen uptake/ 80
kg body weight). Data are derived from 60
Mikkelsen et al.31 and two studies by
Rønnestad and coworkers.34,39 40

20

-20

-40

50 60 70 80 90
-1 -1
Maximal Oxygen Uptake (ml min kg )

decay of acclimation, but should consider adequate re- to both stressors at the same time.43–­45 In contrast, it is not
covery prior to testing to minimize influence from train- straight forward to combine the two acclimation modes
ing or travel fatigue. How the overall stress experienced in terms of the hematological adaptations. Although, it is
by the elite athlete is affected by the additional stress su- clearly attractive to gain both the hypoxia-­related stimu-
perimposed by undertaking heat-­training or going on an lation of erythropoiesis and the plasma volume expan-
altitude camp, should also be considered and the athletes sion with associated Hb-­mass gain from heat-­training, it
guided to account for example, dietary needs (to secure appears that the two may clash if imposed in combina-
iron status, water-­and electrolyte balance.41,42 In prac- tion.8,46 As mentioned previously, altitude exposure typi-
tice this is feasible to implement, if coaches and athletes cally induce an acute reduction in plasma volume, while
for heat-­acclimation use the approach of substituting/al- the opposite response is a significant and presumable
locating part of the less intense part of the weekly/daily important part of the heat-­acclimation required to drive
training to induce heat stress (see our practical guidelines the prolonged hematological response. However, well-­
below) and for altitude accept that power output in gen- controlled studies with sufficient duration are lacking to
eral is lower when exposed to hypoxia. However, with test if the two stressors can be combined (concomitantly
minor adjustments the physiological training stimuli may or one subsequent to the other).
be maintained as discussed above. Another aspect relevant to considerer for the individ-
ual athlete is whether acclimatization to heat or hypoxia
provide the best stimulus in terms of the Hb-­mass gain.
8   |   S H O UL D T H E CYCLIST G O As exemplified for prolonged heat-­training by the vari-
H I G H , G O H OT OR COMB IN E ? ation across athletes in Figure  2 (but not dependent on
the initial blood/plasma volume or training status) and
Considering that the non-­hematological adaptations are observed individual variation across a large number of
specific to the environmental stressor, the choice between heat and altitude camps,2,47 there may be some individ-
heat-­or altitude acclimation may eventually depend on uals responding with a large gain in blood volume, while
the specific exposure scenario for the given stage race. others may have very limited benefit and no change in
For example, if several stages with mountain finishes Hb-­mass. Without, going into a complex discussion on
are located in the first part of the race and the risk of responders/non-­responders (that from a scientific robust
profound heat is low, an altitude camp in the last lead- point of view would require replication of the individual
­in phase may be prioritized. Reversely, if high heat stress responses across several camps and/or testing of sufficient
is expected and flatter stages scheduled in week-­one. The exposure [e.g., longer time or increased intensity required
non-­hematological effects (sudomotor adaptation to heat-­ for that athlete]), it is obvious that some athletes benefit
acclimation and the respiratory response to hypoxia) are more than others from a given intervention. Monitoring
targeting different organs and although there may be individual responses during the first heat or altitude camp
some interference, it is possible for athletes to be adapted are from our point of view relevant, both to identify how
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a given athlete adapts and for subsequent individualized rate at given exercise intensity and the hypoxia-­induced
optimization. stress on muscle metabolism.
Finally, it is very relevant to consider the decay of ac- Staying high enough: preferably above 2500 m as
climation, both for the non-­hematological adaptations residence at lower altitudes may increase the risk of
and the ability to maintain the elevated blood volume the intensity (level of hypoxia) being too low for some
in the period after the acclimation/training camp. The individuals.
fast decay of Hb-­mass following return from altitude to
sea level is indeed a large challenge (and physiological
puzzle15) and the ability to maintain a sufficient hy- 11  |   FOR HEAT ACC LIMATIO N
poxic stimuli may be more difficult that for heat, where WE RECOMMEND
we observe that “maintenance training” with as little
as 3 weekly session (1  h exposures) may be sufficient Sufficient duration: While the non-­hematological adapta-
to preserve the Hb-­mass gain induced by a proceed- tions may be achieved with short-­term protocols (within
ing 5  week intervention.39 The latter implies that heat-­ days) the full potential and Hb-­mass elevation require
training may be integrated in a competition period or prolonged acclimation. We have used ~5 weeks (with at
performed in close proximity to the start of a Grand Tour least 5 weekly sessions) to secure enough time. It remains
without compromising tapering and peaking of perfor- to be tested if 3–­4 weeks with more consistent exposure is
mance. Furthermore, during the stage race the combined sufficient (one study suggest so), but 2 weeks are appar-
environmental-­ exercise heat stress may even on days ently not adequate.
with moderate temperatures be sufficient to prevent or Moderate intensity and duration of the heat stress/
minimize the decay of adaptation.39 level of hyperthermia: In the studies where we have
aimed at core temperatures between 38.5 and 39°C at
the end of ~1 h cycling in heated room or via sweat suit
9   |   A LT I T UDE AN D HE AT-­ training, we observe Hb-­mass adaptations and eleva-
ACC L I M AT I O N T R AIN IN G IN tions in sweat rate that are comparable to studies with
P R ACT I C E AN D POT E N T IALS FOR longer session or more intense heat stress (end core of
I MP ROV E M EN T ~40°C). There thus seems no need to go for longer or
maximal sessions. Sweat rates of 1.5 L/h or above, main-
Both for altitude and as discussed for heat acclimatization, tain RPE (perceived exertion) to moderately hard and
the adequate intensity, duration and consistence of expo- core temperature during the latter part of the session in
sure to elicit the acclimation may be achieved by various the range of 38.5°C will provide sufficient stimulus and
approaches. For specific examples and descriptions on not “overstress” the athletes.
how the level of hypoxia or hyperthermia was controlled, Consistent exposure and maintenance afterward:
we refer to the original studies referenced. Here we will Frequent exposure over a consecutive period is most
provide our best guidance on the parameters of impor- likely advantageous, but once heat-­acclimation has been
tance and how they from our experience in work with achieved athletes may prevent the decay via combining
cyclists (scientific studies and advice of athletes) may be few heat-­ training sessions (e.g., 3 per week—­ or some
implemented in practice. exposures substituted with passive exposure if reduced
training/tapering exclude high volume) with the exercise-­
induced more modest heat stress that most athletes expe-
1 0   |   FO R ALT IT U DE W E rience during normal training/competition.
E M P H A S I Z E T HE IM PORTAN CE OF
FUNDING INFORMATION
Sufficient duration: at least 3 weeks, but preferably longer Lars Nybo and Carsten Lundby are supported by The
as the Hb-­mass response seems to be more consistent and Novo Nordisk Foundation grant to Team Danmark.
keeps increasing with longer exposure.
Consistency of the exposure: To secure sufficient DATA AVAILABILITY STATEMENT
hours/day the cyclists should live and complete the pre- Data sharing is not applicable to this article as no new data
dominant part of the training at altitude. The training were created or analyzed in this study.
routes may naturally take riders to lower altitudes (for
shorter periods), but no need to deliberately go low for ORCID
training. The lower power output and energy turnover at Lars Nybo  https://orcid.org/0000-0002-9090-1958
altitude, seems to be compensated for by elevated heart Bent Rønnestad  https://orcid.org/0000-0002-6907-1347
NYBO et al.   
   9 |

REFERENCES Med Sci Sports Exerc. 2014;46(10):1936-­1945. doi:10.1249/


1. Siebenmann C, Robach P, Lundby C. Regulation of blood vol- MSS.0000000000000321
ume in lowlanders exposed to high altitude. J Appl Physiol 18. Ventura N, Hoppeler H, Seiler R, Binggeli A, Mullis P, Vogt M.
(Bethesda Md 1985). 2017;123(4):957-­966. doi:10.1152/ The response of trained athletes to six weeks of endurance train-
japplphysiol.00118.2017 ing in hypoxia or normoxia. Int J Sports Med. 2003;24(3):166-­
2. Chapman RF. The individual response to training and com- 172. doi:10.1055/s-­2003-­39086
petition at altitude. Br J Sports Med. 2013;47(Suppl 1):i40-­i44. 19. Lundby C, Robach P. Performance enhancement: what are the
doi:10.1136/bjsports-­2013-­092837 physiological limits? Physiology (Bethesda). 2015;30(4):282-­292.
3. Racinais S, Alonso JM, Coutts AJ, et al. Consensus recommen- doi:10.1152/physiol.00052.2014
dations on training and competing in the heat. Scand J Med Sci 20. Jacobs RA, Lundby AKM, Fenk S, et al. Twenty-­eight days of
Sports. 2015;25:6-­19. exposure to 3454 m increases mitochondrial volume density
4. Daanen HAM, Racinais S, Périard JD. Heat acclimation decay in human skeletal muscle. J Physiol. 2016;594(5):1151-­1166.
and Re-­ induction: a systematic review and meta-­ analysis. doi:10.1113/JP271118
Sports Med (Auckl NZ). 2018;48(2):409-­430. doi:10.1007/ 21. Boushel R, Gnaiger E, Calbet JAL, et al. Muscle mitochon-
s40279-­017-­0808-­x drial capacity exceeds maximal oxygen delivery in hu-
5. Lundby C, Montero D, Joyner M. Biology of VO2 max: looking mans. Mitochondrion. 2011;11(2):303-­307. doi:10.1016/j.
under the physiology lamp. Acta Physiol (Oxf). 2017;220(2):218-­ mito.2010.12.006
228. doi:10.1111/apha.12827 22. Jacobs RA, Siebenmann C, Hug M, Toigo M, Meinild AK,
6. Levine BD. VO2max: what do we know, and what do we still Lundby C. Twenty-­eight days at 3454-­m altitude diminishes
need to know? J Physiol. 2008;586(1):25-­34. doi:10.1113/ respiratory capacity but enhances efficiency in human skel-
jphysiol.2007.147629 etal muscle mitochondria. FASEB J. 2012;26(12):5192-­5200.
7. Lundby C, Robach P. Does “altitude training” increase exercise doi:10.1096/fj.12-­218206
performance in elite athletes? Exp Physiol. 2016;101(7):783-­788. 23. Jacobs RA, Boushel R, Wright-­Paradis C, et al. Mitochondrial
doi:10.1113/EP085579 function in human skeletal muscle following high-­ altitude
8. Saunders PU, Garvican-­Lewis LA, Chapman RF, Périard JD. exposure. Exp Physiol. 2013;98(1):245-­255. doi:10.1113/
Special environments: altitude and heat. Int J Sport Nutr Exerc expphysiol.2012.066092
Metab. 2019;29(2):210-­219. doi:10.1123/ijsnem.2018-­0256 24. Gore CJ, Hahn AG, Scroop GC, et al. Increased arterial desatu-
9. Siebenmann C, Hug M, Keiser S, et al. Hypovolemia ex- ration in trained cyclists during maximal exercise at 580 m alti-
plains the reduced stroke volume at altitude. Physiol Rep. tude. J Appl Physiol (Bethesda Md 1985). 1996;80(6):2204-­2210.
2013;1(5):e00094. doi:10.1002/phy2.94 doi:10.1152/jappl.1996.80.6.2204
10. Siebenmann C, Keiser S, Robach P, Lundby C. CORP: the assess- 25. Schuler B, Thomsen JJ, Gassmann M, Lundby C.

ment of total hemoglobin mass by carbon monoxide rebreath- Timing the arrival at 2340 m altitude for aerobic per-
ing. J Appl Physiol (Bethesda Md 1985). 2017;123(3):645-­654. formance. Scand J Med Sci Sports. 2007;17(5):588-­594.
doi:10.1152/japplphysiol.00185.2017 doi:10.1111/j.1600-­0838.2006.00611.x
11. Siebenmann C, Cathomen A, Hug M, et al. Hemoglobin mass 26. Lundby C, Calbet JAL, van Hall G, Saltin B, Sander M.

and intravascular volume kinetics during and after expo- Pulmonary gas exchange at maximal exercise in Danish low-
sure to 3,454-­m altitude. J Appl Physiol (Bethesda Md 1985). landers during 8 wk of acclimatization to 4,100 m and in high-­
2015;119(10):1194-­1201. doi:10.1152/japplphysiol.01121.2014 altitude Aymara natives. Am J Physiol Regul Integr Comp Physiol.
12. Rasmussen P, Siebenmann C, Díaz V, Lundby C. Red cell
2004;287(5):R1202-­R1208. doi:10.1152/ajpregu.00725.2003
volume expansion at altitude: a meta-­ analysis and Monte 27. Tyler CJ, Reeve T, Hodges GJ, Cheung SS. The effects of heat
Carlo simulation. Med Sci Sports Exerc. 2013;45(9):1767-­1772. adaptation on physiology, perception and exercise performance
doi:10.1249/MSS.0b013e31829047e5 in the heat: a meta-­analysis. Sports Med. 2016;46(11):1699-­1724.
13. Siebenmann C, Robach P, Jacobs RA, et al. “Live high-­
doi:10.1007/s40279-­016-­0538-­5
train low” using normobaric hypoxia: a double-­ blinded, 28. Périard JD, Eijsvogels TMH, Daanen HAM. Exercise under heat
placebo-­controlled study. J Appl Physiol (Bethesda Md 1985). stress: thermoregulation, hydration, performance implications,
2012;112(1):106-­117. doi:10.1152/japplphysiol.00388.2011 and mitigation strategies. Physiol Rev. 2021;101(4):1873-­1979.
14. Robach P, Hansen J, Pichon A, et al. Hypobaric live high-­train doi:10.1152/physrev.00038.2020
low does not improve aerobic performance more than live 29. Karlsen A, Nybo L, Nørgaard SJ, Jensen MV, Bonne T, Racinais
low-­train low in cross-­country skiers. Scand J Med Sci Sports. S. Time course of natural heat acclimatization in well-­
2018;28(6):1636-­1652. doi:10.1111/sms.13075 trained cyclists during a 2-­week training camp in the heat.
15. Klein M, Kaestner L, Bogdanova AY, et al. Absence of neocytol- Scand J Med Sci Sports. 2015;25(Suppl 1):240-­249. doi:10.1111/
ysis in humans returning from a 3-­week high-­altitude sojourn. sms.12449
Acta Physiol (Oxf). 2021;232(3):e13647. doi:10.1111/apha.13647 30. Karlsen A, Racinais S, Jensen MV, Nørgaard SJ, Bonne T, Nybo
16. Levine BD, Stray-­
Gundersen J. “Living high-­ training low”: L. Heat acclimatization does not improve VO2max or cycling
effect of moderate-­altitude acclimatization with low-­altitude performance in a cool climate in trained cyclists. Scand J Med
training on performance. J Appl Physiol (Bethesda Md 1985). Sci Sports. 2015;25(Suppl 1):269-­276. doi:10.1111/sms.12409
1997;83(1):102-­112. doi:10.1152/jappl.1997.83.1.102 31. Mikkelsen CJ, Junge N, Piil JF, et al. Prolonged heat acclima-
17. Robach P, Bonne T, Flück D, et al. Hypoxic training: effect on tion and aerobic performance in endurance trained athletes.
mitochondrial function and aerobic performance in hypoxia. Front Physiol. 2019;10:1372. doi:10.3389/fphys.2019.01372
|
10       NYBO et al.

32. Keiser S, Flück D, Hüppin F, Stravs A, Hilty MP, Lundby C. 42. Michalczyk M, Czuba M, Zydek G, Zając A, Langfort J.

Heat training increases exercise capacity in hot but not in tem- Dietary recommendations for cyclists during altitude training.
perate conditions: a mechanistic counter-­balanced cross-­over Nutrients. 2016;8(6):E377. doi:10.3390/nu8060377
study. Am J Physiol Heart Circ Physiol. 2015;309(5):H750-­H761. 43. McCleave EL, Slattery KM, Duffield R, et al. Impaired heat
doi:10.1152/ajpheart.00138.2015 adaptation from combined heat training and “live high, train
33. Rønnestad BR, Lid OM, Hansen J, et al. Heat suit training low” hypoxia. Int J Sports Physiol Perform. 2019;14(5):635-­643.
increases hemoglobin mass in elite cross-­ country skiers. doi:10.1123/ijspp.2018-­0399
Scand J Med Sci Sports. 2022;32(7):1089-­1098. doi:10.1111/ 44. Hanson ED, Cooke MB, Anderson MJ, Gerber T, Danaher JA,
sms.14156 Stathis CG. Heat acclimation with or without Normobaric hy-
34. Rønnestad BR, Hamarsland H, Hansen J, et al. Five weeks of poxia exposure leads to similar improvements in endurance
heat training increases haemoglobin mass in elite cyclists. Exp performance in the heat. Sports (Basel Switz). 2022;10(5):69.
Physiol. 2021;106(1):316-­327. doi:10.1113/EP088544 doi:10.3390/sports10050069
35. Oberholzer L, Siebenmann C, Mikkelsen CJ, et al. Hematological 45. Sotiridis A, Miliotis P, Ciuha U, Koskolou M, Mekjavic IB. No
adaptations to prolonged heat acclimation in endurance-­ ergogenic effects of a 10-­day combined heat and hypoxic accli-
trained males. Front Physiol. 2019;10:1379. doi:10.3389/ mation on aerobic performance in normoxic thermoneutral or
fphys.2019.01379 hot conditions. Eur J Appl Physiol. 2019;119(11–­12):2513-­2527.
36. Minson CT, Cotter JD. Rebuttal by Christopher T. Minson
doi:10.1007/s00421-­019-­04215-­5
and James D. Cotter. J Physiol. 2016;594(2):249. doi:10.1113/ 46. McCleave EL, Slattery KM, Duffield R, et al. Temperate perfor-
JP271670 mance benefits after heat, but not combined heat and hypoxic
37. Nybo L, Lundby C. CrossTalk opposing view: heat acclimatiza- training. Med Sci Sports Exerc. 2017;49(3):509-­517. doi:10.1249/
tion does not improve exercise performance in a cool condition. MSS.0000000000001138
J Physiol. 2016;594(2):245-­247. doi:10.1113/JP270880 47. Racinais S, Mohr M, Buchheit M, et al. Individual responses
38. Lorenzo S, Halliwill JR, Sawka MN, Minson CT. Heat ac-
to short-­term heat acclimatisation as predictors of football
climation improves exercise performance. J Appl Physiol performance in a hot, dry environment. Br J Sports Med.
(Bethesda Md 1985). 2010;109(4):1140-­1147. doi:10.1152/ 2012;46(11):810-­815. doi:10.1136/bjsports-­2012-­091227
japplphysiol.00495.2010
39. Rønnestad BR, Urianstad T, Hamarsland H, et al. Heat train-
ing efficiently increases and maintains hemoglobin mass
and temperate endurance performance in elite cyclists. How to cite this article: Nybo L, Rønnestad B,
Med Sci Sports Exerc. 2022;54(9):1515-­1526. doi:10.1249/ Lundby C. High or hot—­Perspectives on altitude
MSS.0000000000002928 camps and heat-acclimation training as preparation
40. Rønnestad BR, Hansen J, Bonne TC, Lundby C. Case report:
for prolonged stage races. Scand J Med Sci Sports.
heat suit training may increase hemoglobin mass in elite
2022;00:1-10. doi: 10.1111/sms.14268
athletes. Int J Sports Physiol Perform. 2022;17(1):115-­119.
doi:10.1123/ijspp.2021-­0033
41. Hinton PS. Iron and the endurance athlete. Appl Physiol Nutr
Metab Physiol Appl Nutr Metab. 2014;39(9):1012-­1018. doi:10.​
1139/apnm-­2014-­0147

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