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52 Current Allergy & Clinical Immunology, June 2010 Vol 23, No. 2
re s p i r a t o r y t r a C t s y m p t o m s i n
e n d u r a n C e a t h l e t e s – a r e v i e w o f
C a u s e s a n d C o n s e q u e n C e s
It is well established that medical conditions can be
associated with endurance physical activities and
that respiratory tract symptoms (RTS) is one of the
more common medical conditions that is encoun-
tered in these athletes. RTS are particularly during
intense training and immediately after competition.
There are many studies documenting that alterations
in immune parameters occur in athletes undergoing
intense training and competition. It is a common as-
sumption that RTS in endurance athletes are as a
result of infections during periods where there are
known alterations in immune parameters. However,
there are no studies directly linking alterations in
immune parameters in response to training and
documented evidence of infections in athletes. Al-
lergic conditions, in particular allergic rhinitis, are also
common in endurance athletes, and there is some
overlap in the symptomatology of upper respiratory
tract infection (URTI) and allergic rhinitis. Chronic
allergic rhinitis may also predispose to the develop-
ment of URTI. The infective hypothesis, the allergic
hypothesis and alternate hypotheses to explain the
high prevalence of RTS in endurance athletes require
further investigation. Current clinical guidelines for
the management of RTS in athletes are mainly based
on the assumption that RTS in athletes are only as a
result of an infective cause. If other causes for RTS
in athletes are documented, these guidelines may
Correspondence to: Prof Martin Schwellnus, e-mail firstname.lastname@example.org
MP Schwellnus, MB BCh, MSc (Med) Sports
Science, MD (Sports and Exercise Medicine), FACSM,
M Lichaba, MB ChB, MPhil (Sports Medicine)
EW Derman, MB ChB, PhD (Sports and Exercise
Medicine), FACSM, FFIMS
UCT/MRC Research Unit for Exercise Science and
Sports Medicine, Department of Human Biology,
University of Cape Town, International Olympic Com-
mittee Research Centre, Cape Town, South Africa
It is well established that regular exercise training is
beneﬁcial in the primary and secondary prevention of
chronic diseases of lifestyle.1-3 There is therefore a
perception that athletes are generally healthy individu-
als, and that exercise training also protects against
the risk of acquiring acute medical illnesses, includ-
ing infections.4,5 However, epidemiological evidence
shows that increased exercise training (volume and
intensity), particularly in endurance athletes, can be as-
sociated with an increased risk of developing respira-
tory tract symptoms (RTS) that may be associated with
This review paper focuses on the medical conditions
that affect the respiratory system in endurance athletes,
and more speciﬁcally the possible mechanisms that
may lead to the development of RTS. These symptoms
can occur at various stages of training and competition:
the pre-competition period (during the preparation train-
ing period), during the competition (intra-competition),
or the post-competition recovery period (from immedi-
ately after the ﬁnish up to 2-6 weeks later).
Terminology and deﬁnitions
Endurance athletes can present with RTS ranging
from ‘blocked nose’, ‘runny nose’, sore throat, swollen
glands, cough, wheeze to chest pain. These symptoms
may be accompanied by additional systemic symptoms
such as fever, headache, muscle aches, joint pains and
general fatigue. In some instances the term ‘ﬂu-like’ ill-
ness has been used for RTS which are accompanied
by systemic symptoms. In most studies where these
RTS, or more speciﬁcally upper respiratory tract symp-
toms (URTS), have been documented, these were
self-reported by athletes, without any evidence of ac-
tual infection.15 We are aware of only a few studies in
which attempts have been made to obtain actual evi-
dence of an infective agent in athletes presenting with
RTS.14,16-18 Therefore, the general use of the term up-
per respiratory tract infections (URTI), as has been used
in many reports, without documenting actual evidence
that these symptoms are due to an infection, may well
At present, it is well recognised that an athlete present-
ing with RTS that are localised to the upper airways
(nose and orophraynx) is given different medical ad-
vice about exercise and training, when compared with
an athlete presenting with RTS below the orophraynx
(cough, wheeze, chest pain), or athletes presenting
with accompanying systemic symptoms such as fever,
myalgia, arthralgia and general fatigue.7 This clinical
test has also been referred to as the ‘neck check’.19-21
The use of the terms upper respiratory tract symptoms
(URTS) (‘blocked nose’, ‘runny nose’, sore throat, swol-
len glands), lower respiratory tract symptoms (LRTS)
(cough, wheeze, chest pain) and systemic symptoms
(SS) (fever, myalgia, arthralgia, general fatigue) to de-
scribe these clinical presentations is therefore more ap-
For the purposes of this paper, the following terminol-
ogy is used:
• Upper respiratory tract symptoms (URTS) refer
to the presence of respiratory symptoms that are
localised to the nose and pharynx (‘blocked nose’,
‘runny nose’, sore throat)
• Lower respiratory tract symptoms (LRTS) refer
to the presence of respiratory symptoms below the
level of the phraynx (cough, wheeze, chest pain)
• Systemic symptoms (SS) of infection refer to
symptoms such as fever, myalgia, arthralgia and
general fatigue that may accompany infections.
It should be pointed out that we are fully aware of the
fact that RTS in athletes could also be due to many
other cardiorespiratory conditions. In particular, we rec-
ognise that asthma is a very common respiratory condi-
Current Allergy & Clinical Immunology, June 2010 Vol 23, No. 2 53
tion in athletes that could give rise to RTS. However, in
this paper we wish to conﬁne the discussions to RTS
that have been related to infections, and the main focus
is on URTS. We also acknowledge that the SS listed
above can also occur as a result of many other infec-
tions (not only those affecting the respiratory tract) and
other systemic conditions.
EPIDEMIOLOGY OF RTS IN ENDURANCE
Respiratory tract infections (RTI), in particular URTI, are
very common in the general population,22 and are more
likely to affect individuals in the extremes of age and
the immune-compromised individual.23 It has been re-
ported that 75-80% of all acute morbidities in the popu-
lation of the USA are due to respiratory disease, 80% of
which are due to viral infections of the respiratory tract,
with an average of 3-6 respiratory tract illnesses per
person per year.22,24 URTI are the most common types
of infection, and are mainly caused by viruses.22
In athletes, it has also been reported that URTI (com-
monly caused by viruses) are by far the leading cause of
infectious diseases in the training room.22 A number of
studies have documented URTS in endurance athletes,
including runners,25-29 cyclists,14 cross-country skiers,30
swimmers,12,31,32 rowers,33 and in participants of other
sports such as tennis players,34, gymnasts,35 wheel-
chair athletes,36 and even in those undergoing military
training.37 It is very important to note that in all these
studies, there is no veriﬁcation that the symptoms are
due to an infection. Hence, in all these studies it is cor-
rect to describe these as symptoms of URTI rather than
actually documented URTI. The term URTS is therefore
used consistently in this paper, when referring to these
The risk of developing URTS in athletes has been
reviewed.6,13,38 In one of the ﬁrst studies to document
the relationship between URTS and endurance ex-
ercise, Peters and Bateman25 in 1983 found that the
incidence of URTS was twice as high in ultradistance
runners in the ﬁrst 10-14 days following an endurance
race, when compared with suitable sedentary controls
followed up in the same time period. These researchers
also reported that the incidence of URTS was higher
among the faster runners.
Following that ﬁrst report, there have been a number of
retrospective,11,39,40 and prospective14,17,18,26,27,36,41-43
studies documenting URTS in different groups of ath-
letes. An in-depth discussion of the ﬁndings of all these
studies is beyond the scope of this review. However, a
summary of the main ﬁndings from these studies is as
• Following endurance events (mainly ultramarathon
running) athletes experience an increased incidence
of URTS compared with sedentary controls.25,27,39
durance athletes over months show that increased
training is associated with an increased risk of
• Some studies report other factors that increase an
athlete’s risk of developing URTS including female
gender,11,26 decreased vitamin C intake,27 perceived
stress,11 sleep deprivation,11 and lack of awareness
ing resulted in increased natural-killer-cell function,
increased T-cell function and reduced incidence of
Over the past decade, the results of studies in athletes
and other populations have led to the commonly accept-
ed hypothesis that the relationship between exercise
training and risk of URTS is a ‘J’-shaped curve.11,19,44,45
It appears that physical inactivity is associated with an
increased risk of URTS,46 while moderate intensity and
duration of physical activity has been shown to be pro-
tective in some10,47-50 but not in all studies.51,52 How-
ever, high-intensity, prolonged exercise, such as during
endurance training and competition, may increase the
risk of developing URTS.11,26,41,53
AETIOLOGY AND PATHOPHYSIOLOGY OF
RTS IN ENDURANCE ATHLETES
Until recently, it was generally assumed that RTS in
athletes were due to an infective cause, and that this
increased risk of infection was because prolonged, in-
tense training or competition has been associated with
a ‘suppression’ of a variety of parameters in the immune
system. The ‘suppression’ of immune parameters in
the 3-72 hours following intense and prolonged training
has been termed the ‘open window’ period. During this
period, it is hypothesised that infective agents entering
the URT would cause URTI. Additional factors that may
increase the risk of infection are the large volumes of air
entering the respiratory tract particularly when mouth
breathing is used by athletes during high-intensity exer-
cise54 and nutritional deﬁciencies, in particular carbohy-
drate55 and vitamin C deﬁciency.28,29,56-58
However, it is also well established that RTS are not
always due to an infection and that there may be
other causes for these symptoms such as allergies
or inﬂammation caused by other physical or chemical
irritants.12,17,18,59 It is only more recently that other
possible causes of URTS in athletes during training or
competition have been proposed. The possible hypoth-
eses for the cause of RTS in endurance athletes are
discussed under the following headings: infective hy-
pothesis, allergic hypothesis, and other causes. Scien-
tiﬁc evidence for each of these is brieﬂy reviewed.
Infective hypothesis for RTS in athletes
Since 1990, the relationship between an acute exer-
cise bout and immune parameters, as well as the re-
lationship between exercise training and changes in
the immune parameters, has received more and more
attention. Over the past 10-15 years, the number of
publications in this ﬁeld have increased by more than
10-fold.60 There is now an extensive body of knowl-
edge documenting the relationship between exercise
and the immune system and this has been reviewed in
a number of publications.5,8,15,60-65 The main focus of
this review is not on exercise immunology, and hence
an in-depth review of the interaction between exercise
and the immune system is beyond the scope of this
review. However, the main current ﬁndings relating to
changes in the immune system as a result of exercise,
and how these may relate to RTS in athletes are brieﬂy
It is well established that an acute bout of exercise as
well as exercise training can alter a variety of immune
parameters. Changes in systemic immunity,5 mucosal
immunity, and cytokines62 in response to exercise have
been reviewed.66 To date, there have been numerous
studies that were conducted to relate these changes in
immune parameters to URTS in athletes. However, in
most of these studies, no direct relationship between
changes in immune parameters and the presence of
URTS could be documented. This lack of association
between measures of immune function and URTS was
ﬁrst pointed out by Shephard in 2000,15 and again more
recently.60,63 The evidence for a direct link between ob-
served changes in immune parameters, and the devel-
opment of URTS can be summarised as follows:
54 Current Allergy & Clinical Immunology, June 2010 Vol 23, No. 2
training can alter systemic 8,33,42,43,67-72 and mucosal
immunity34,35,37,47,73-81 by enhancing some param-
eters and suppressing others.
immune system is not well established, and requires
eters and the development of RTS in athletes has
been examined,31,34,35,37,70,74,75,79,82 but to date, no
consistent cause-effect relationship has been docu-
• Nutritional interventions to change immune system
parameters and decrease the risk of URTS in athletes
have been reviewed.83,84
• Althoughtheeffectof nutritionalsupplementssuch
as carbohydrates,55 glutamine,85 and vitamin C28,29,56-58
on immune parameters have been studied,86-89 with
the exception of vitamin C supplementation,27 none
of the other supplements has been shown to de-
crease URTS in athletes.55,87
• There is early experimental evidence from one
study90 to suggest that the use of probiotics may be
of value in reducing the duration and severity of RTS
in endurance athletes, perhaps by modulating the im-
mune response to exercise training.91
It is therefore clear that the relationship between exer-
cise-induced changes in immune parameters and the
development of RTS in athletes is not well established.
Furthermore, there are no studies conﬁrming the diag-
nosis of an infection in athletes presenting with URTS
where either serological criteria have been used, or
where actual pathogens have been cultured. In conclu-
sion, scientiﬁc evidence supporting the infective hy-
pothesis as the cause of URTS in athletes undergoing
training or competition is lacking. Alternative hypothe-
ses, perhaps linking changes in the immune system pa-
rameters during intense exercise, and the development
of RTS have to be considered. It has been suggested
that allergic disorders, which are also mediated through
the immune system, may account for the development
of at least some RTS in athletes. This hypothesis will
now be explored.
Allergic hypothesis for RTS in athletes
It is well established that allergies are very common
worldwide and that the prevalence of allergies has in-
creased over the last few decades.92,93 The prevalence
of allergic diseases in the population of industrialised
countries has been estimated at 10-25%. As men-
tioned, allergies have increased signiﬁcantly over the
last 50 years in developed countries, probably as a re-
sult of air pollution.94 There is a very wide spectrum
of clinical presentations of allergic conditions, ranging
from a benign rash to exercise-induced anaphylaxis.95
Allergic conditions of the respiratory tract in athletes
can vary from allergic sinusitis, allergic rhinitis, allergic
rhinoconjunctivitis to allergic asthma, and these condi-
tions have been reviewed in other papers in this issue
of the journal.93,96-99 In summary, there is evidence that
allergies are common in elite athletes with the preva-
lence of any allergy varying between 16% and 32%.
For the purposes of this review paper, it is important
to note that the clinical presentation of allergic condi-
tions that affect the respiratory tract may mimic those
of URTI. Common URTS that could be due to either
infections or allergies are ‘blocked nose’ and ‘runny
nose’, while more systemic symptoms, such as head-
ache, malaise and fatigue, can also occur as a result of
allergies.93 Associated symptoms, such as itchy nose,
sneezing and itchy runny eyes, are more likely due to
allergic than infective causes.54,98,100 However, chronic
allergies can, similarly to infections, also result in im-
paired sports performance; the mechanisms underlying
this effect have been described in this edition of the
journal.93,101 It can be therefore be hypothesised that
URTS in endurance athletes may be related to allergies
rather than being infective in nature, or there may be
an interaction between these two mechanisms. There
may well be a continuum of URT disease with an over-
lap between respiratory tract allergies and infections,
which has to date not been explored.
Other hypotheses for RTS in athletes
Any discussion of the possible causes of RTS in ath-
letes will not be complete unless it is mentioned that
many other irritants can also cause an inﬂammatory
response in the respiratory tract. A non-allergic, non-
infective rhinitis can be caused by physical factors.
Physical factors that may cause RTS in athletes include
high ventilatory rate, cold, dry air, increased air turbu-
lence, mouth-breathing, and inhaled irritants (physical,
chemical and allergens).12,17 When the ventilatory rate
exceeds 30 l/min there is a tendency towards both
mouth breathing and nasal breathing and this causes
deposition of airborne allergens and irritants in the up-
per and lower respiratory tracts.54 Pollutant irritants are
classiﬁed as primary or secondary. Primary pollutants
are directly from the source such as inorganic gases.
Secondary pollutants result from chemical reactions
of emitted and natural precursors. Pollutants of major
concern to respiratory health are sulphur dioxide (SO2),
photochemical smog (ozone and nitrogen dioxide, NO2)
and airborne particulates.94 Recently, it has been docu-
mented that there is an increase in airway inﬂamma-
tory cells, possibly related to increased ventilation of
cold and dry air.102,103 The precise relationship between
these observed inﬂammatory cells and respiratory tract
pathology in athletes requires further investigation.102 It
is important to point out that other hypotheses relating
physical and chemical factors to RTS in athletes may
require further study.
Summary: Hypotheses for the aetiology of
RTS in athletes
In summary, the precise aetiology and pathogenesis of
RTS in athletes during training, and immediately after
intense competition is not clear. Until recently, the pre-
vailing hypothesis for the high incidence of mainly URTS
in endurance athletes following competition was that
alterations in the immune system postexercise cause
infections. However, actual infection has never been
documented either clinically, by serological means, or
through culture of organisms. Furthermore, despite nu-
merous attempts, no clear relationship between altered
immune parameters and URTS has been documented.
Therefore, the infective hypothesis for RTS in athletes
requires further study, or alternative hypotheses have
to be considered.
Concomitantly, it has been documented that respira-
tory tract allergies, in particular allergic rhinitis, are com-
mon in athletes, especially in endurance athletes. The
symptoms of allergic conditions of the URT and the
symptoms of URTI overlap, and the possibility that RTS
in endurance athletes is related to allergies has to be
considered. Finally, other physical factors causing RTS
in athletes must not be disregarded.
Current Allergy & Clinical Immunology, June 2010 Vol 23, No. 2 55
EFFECTS OF RTS ON TRAINING AND COM-
PETITION IN ENDURANCE ATHLETES
The effect of RTS on training and performance has not
been well investigated. This is probably because the
aetiology of RTS in athletes is not established. The ef-
fects of both RTI and allergic conditions of the respira-
tory tract on training and athletic performance will now
There are only a few studies where the effects of
RTI on training and performance have been exam-
ined. The main reason for this is that although very
rare, some infective agents can cause an associated
myocarditis.22,104-106 Viral myocarditis has been the
cause of sudden death in athletes.105,106 Therefore, the
current guideline for athletes with documented RTS is
to avoid training if there are any symptoms of possible
concomitant myocarditis, such as chest pain, short-
ness of breath at rest, resting tachycardia, or systemic
symptoms, such as fever, myalgia or joint pain. If any of
these symptoms are present, athletes are advised not
to train at all based on clinical evidence.22 For obvious
ethical reasons the validity of this advice has not been
studied systematically.7 If symptoms are localised to
the URT, athletes frequently do not seek medical assis-
tance and, according to anecdotal evidence, many con-
tinue training. However, the effects of these localised
URTS on training and performance have not been well
The effects of febrile illness on muscle function in hu-
mans have been investigated in a few studies. In one
study where a fever was induced in seven volunteers
by inoculation with the sandﬂy fever virus, it was doc-
umented that there is a transient decrease in muscle
function which correlated with myalgia, rather than the
presence of fever.107 In this study, it was not possible
to distinguish between inactivity (bed rest) or the febrile
illness as the main cause of loss of muscle strength.
In another study by the same investigators, isometric
muscle strength and isometric muscle endurance were
recorded serially (during fever, after fever, at 1 and 4
months after the infection) at the time of an acute infec-
tious disease of viral or mycoplasmal aetiology in over
30 young men. In this study, the febrile illness resulted
in a 5-15% decrease in isometric muscle strength and
a 13-18% decrease in isometric muscle endurance as
compared with control subjects undergoing bed rest for
the same time period as the infected subjects.108,109 It
is important to point out that in these studies the infec-
tion was clearly documented, and that it was associ-
ated with SS (fever). The effects of a localised URTI on
exercise performance and training have to our knowl-
edge not been studied, other than in a report where
URTI was the main medical reason for absence from
training in elite skiers.30
CLINICAL ADVICE TO ATHLETES PRE-
SENTING WITH RTS
The clinical advice that is currently given to athletes pre-
senting with RTS is largely based on whether the RTS
are conﬁned to the upper airways (above the neck), or
whether there are LRTS or SS (below the neck). This
clinical test has been termed the ‘neck check’.19-22 The
main reasons for adopting this clinical approach are
twofold. Firstly, LRTS or SS may indicate a generalised
(systemic) infection, and systemic viral or bacterial in-
fections may be associated with myocarditis, and this
is a potential cause of sudden death in an exercising
athlete.22,104,105 Secondly, as has been discussed, there
are indications that exercise performance is impaired
signiﬁcantly when LRTS or SS are present.
Therefore the current clinical approach when athletes
present with RTS is to document localised (‘runny
nose’, ‘blocked nose’, sore throat) or additional LRTS
(cough, chest pain, wheeze) or SS (muscle aches, joint
pain, fever, fatigue). If only localised symptoms are
present, moderate intensity exercise is allowed for a
short duration, and depending on how the athlete feels,
this can be continued. In the presence of any LRTS or
SS exercise is not allowed and follow-up clinical assess-
ment is advocated.19-22
However, in this current clinical approach, the pres-
ence or absence of allergic symptoms and their man-
agement, which is different to that of URTI,93,98,100 are
largely ignored. If a closer association between RTS
in athletes undergoing intense training and allergies is
documented, this current clinical approach may have to
SUMMARY AND CONCLUSIONS
cal activities are common.
that is encountered in endurance athletes, particu-
larly during intense training and immediately after
• There are many studies documenting alterations in
immune parameters in athletes undergoing intense
training and competition.
• It is a common assumption that RTS in endurance
athletes are as a result of infections during periods
where there are known alterations in immune param-
mune parameters in response to training and docu-
mented evidence of infections in athletes.
• Allergic conditions, in particular allergic rhinitis, are
common in endurance athletes.
• There is some overlap in the symptomatology of
URTI and allergic rhinitis.
opment of URT infections.
alternative hypotheses to explain the high prevalence
of RTS in endurance athletes require further investi-
• Current clinical guidelines for the management of
RTS in athletes are mainly based on the assumption
that RTS in athletes are only as a result of an infective
• Ifother causesforRTSinathletesaredocumented,
these guidelines may require modiﬁcation.
Declaration of conﬂict of interest
The authors declare no conﬂict of interest.
1. Warburton DE, Nicol CW, Bredin SS. Health beneﬁts of physical
activity: the evidence. CMAJ 2006; 174: 801-809.
2. Karacabey K. Effect of regular exercise on health and disease. Neu-
ro Endocrinol Lett 2005; 26: 617-623.
3. Kohl HW, III. Physical activity and cardiovascular disease: evidence
for a dose response. Med Sci Sports Exerc 2001; 33(6 Suppl): S472-
4. Brenner IK, Shek PN, Shephard RJ. Infection in athletes. Sports
Med 1994; 17: 86-107.
5. Nieman DC. Special feature for the Olympics: effects of exercise
on the immune system: exercise effects on systemic immunity. Im-
munol Cell Biol 2000; 78: 496-501.
6. Schumacher YO, Pottgiesser T, Koenig D. The risk of upper respira-
tory tract infections (URTI) in athletes. International Sportmed Jour-
nal 2003; 4: 1-12.
56 Current Allergy & Clinical Immunology, June 2010 Vol 23, No. 2
7. Friman G, Wesslen L. Special feature for the Olympics: effects of
exercise on the immune system: infections and exercise in high-
performance athletes. Immunol Cell Biol 2000; 78: 510-522.
8. Lakier SL. Overtraining, excessive exercise, and altered immunity:
is this a T helper-1 versus T helper-2 lymphocyte response? Sports
Med 2003; 33: 347-364.
9. Nieman DC. Is infection risk linked to exercise workload? Med Sci
Sports Exerc 2000; 32(7 Suppl):S406-S411.
10. Calabrese LH, Nieman DC. Exercise, immunity, and infection. J Am
Osteopath Assoc 1996; 96: 166-176.
11. Konig D, Grathwohl D, Weinstock C, Northoff H, Berg A. Upper re-
spiratory tract infection in athletes: inﬂuence of lifestyle, type of
sport, training effort, and immunostimulant intake. Exerc Immunol
Rev 2000; 6: 102-120.
12. Bougault V, Turmel J, Levesque B, Boulet LP. The respiratory health
of swimmers. Sports Med 2009; 39: 295-312.
13. Moreira A, Delgado L, Moreira P, Haahtela T. Does exercise increase
the risk of upper respiratory tract infections? Br Med Bull 2009; 90:
14. Spence L, Brown WJ, Pyne DB, et al. Incidence, etiology, and symp-
tomatology of upper respiratory illness in elite athletes. Med Sci
Sports Exerc 2007; 39: 577-586.
15. Shephard RJ. Special feature for the Olympics: effects of exercise
on the immune system: overview of the epidemiology of exercise
immunology. Immunol Cell Biol 2000; 78: 485-495.
16. Schwellnus M P, Kiessig M, Derman W, Noakes T D. Fusafungine
reduces symptoms of upper respiratory tract infections (URTI)
in runners after a 56km race. Med Sci Sports Exerc 1997; 29(5
17. Cox AJ, Gleeson M, Pyne DB, Callister R, Hopkins WG, Fricker PA.
Clinical and laboratory evaluation of upper respiratory symptoms in
elite athletes. Clin J Sport Med 2008; 18: 438-445.
18. Bermon S. Airway inﬂammation and upper respiratory tract infec-
tion in athletes: is there a link? Exerc Immunol Rev 2007; 13: 6-14.
19. Nieman DC. Current perspective on exercise immunology. Curr
Sports Med Rep 2003; 2: 239-242.
20. Metz JP. Upper respiratory tract infections: who plays, who sits?
Curr Sports Med Rep 2003; 2: 84-90.
21. Eichner E R. Infection, immunity, and exercise: what to tell patients.
Phys Sports Med 1993; 21: 125-135.
22. Hosey RG, Rodenberg RE. Training room management of medical
conditions: infectious diseases. Clin Sports Med 2005; 24: 477-506,
23. Kostka T, Berthouze SE, Lacour J, Bonnefoy M. The symptoma-
tology of upper respiratory tract infections and exercise in elderly
people. Med Sci Sports Exerc 2000; 32: 46-51.
24. Ray CG. Inﬂuenza. Respiratory syncytial virus, adenovirus, and other
respiratory viruses. In: Ryan KJ, ed. Sherris Medical Microbiology
An Introduction to Infectious Diseases. 3rd ed. Upper Saddle River:
Prentice Hall, 1994: 451-466.
25. Peters EM, Bateman ED. Ultramarathon running and upper respira-
tory tract infections. An epidemiological survey. S Afr Med J 1983;
26. Heath GW, Ford ES, Craven TE, Macera CA, Jackson KL, Pate RR.
Exercise and the incidence of upper respiratory tract infections.
Med Sci Sports Exerc 1991; 23: 152-157.
27. Peters EM, Goetzsche JM, Grobbelaar B, Noakes TD. Vitamin C
supplementation reduces the incidence of postrace symptoms of
upper-respiratory-tract infection in ultramarathon runners. Am J Clin
Nutr 1993; 57: 170-174.
28. Peters EM, Anderson R, Nieman DC, Fickl H, Jogessar V. Vitamin
C supplementation attenuates the increases in circulating cortisol,
adrenaline and anti-inﬂammatory polypeptides following ultramara-
thon running. Int J Sports Med 2001; 22: 537-543.
29. Peters EM, Anderson R, Theron AJ. Attenuation of increase in cir-
culating cortisol and enhancement of the acute phase protein re-
sponse in vitamin C-supplemented ultramarathoners. Int J Sports
Med 2001; 22: 120-126.
30. Berglund B, Hemmingsson P. Infectious disease in the elite cross-
country skiers: a one-year incidence study. Clinical Sports Medicine
1990; 2: 19-23.
31. Gleeson M, McDonald WA, Pyne DB, et al. Immune status and re-
spiratory illness for elite swimmers during a 12- week training cycle.
Int J Sports Med 2000; 21: 302-307.
32. Gleeson M, Pyne DB, Austin JP, et al. Epstein-Barr virus reactiva-
tion and upper-respiratory illness in elite swimmers. Med Sci Sports
Exerc 2002; 34: 411-417.
33. Nieman DC, Nehlsen-Cannarella SL, Fagoaga OR, et al. Immune
function in female elite rowers and non-athletes. Br J Sports Med
2000; 34: 181-187.
34. Novas AM, Rowbottom DG, Jenkins DG. Tennis, incidence of URTI
and salivary IgA. Int J Sports Med 2003; 24: 223-229.
35. Filaire E, Bonis J, Lac G. Relationships between physiological and
psychological stress and salivary immunoglobulin A among young
female gymnasts. Percept Mot Skills 2004; 99: 605-617.
36. Furusawa K, Tajima F, Okawa H, Takahashi M, Ogata H. The inci-
dence of post-race symptoms of upper respiratory tract infection in
wheelchair marathon racers. Spinal Cord 2007; 45: 513-517.
37. Tiollier E, Gomez-Merino D, Burnat P, et al. Intense training: mucosal
immunity and incidence of respiratory infections. Eur J Appl Physiol
2005; 93: 421-428.
38. Page CL, Diehl JJ. Upper respiratory tract infections in athletes.
Clinical Sports Medicine 2007; 26: 345-359.
39. Nieman DC, Johanssen L M, Lee J W. Infectious episodes in run-
ners before and after a roadrace. J Sports Med Phys Fitness 1989;
40. Fricker PA, Gleeson M, Flanagan A, et al. Do elite swimmers expe-
rience more upper respiratory tract illness than nonathletes? Clin
Exerc Physiol 2000; 2: 155-158.
41. Linde F. Running and upper respiratory tract infections. Scan
J Sports Sci 1987; 9: 21-23
42. Nieman DC, Nehlsen-Cannarella SL, Markoff PA, et al. The effects
of moderate exercise training on natural killer cells and acute upper
respiratory tract infections. Int J Sports Med 1990; 11: 467-473.
43. Nieman DC, Henson DA, Gusewitch G, et al. Physical activity and
immune function in elderly women. Med Sci Sports Exerc 1993; 25:
44. Baum M, Liesen H. [Sports and the immune system]. Orthopade
1997; 26: 976-980.
45. Nieman DC. Exercise, infection, and immunity. Int J Sports Med
1994; 15 Suppl 3: S131-S141.
46. Jedrychowski W, Maugeri U, Flak E, Mroz E, Bianchi I. Cohort study
on low physical activity level and recurrent acute respiratory infec-
tions in schoolchildren. Cent Eur J Public Health 2001; 9: 126-129.
47. Klentrou P, Cieslak T, MacNeil M, Vintinner A, Plyley M. Effect of
moderate exercise on salivary immunoglobulin A and infection risk
in humans. Eur J Appl Physiol 2002; 87: 153-158.
48. Klentrou P, Hay J, Plyley M. Habitual physical activity levels and
health outcomes of Ontario youth. Eur J Appl Physiol 2003; 89: 460-
49. Kotaniemi-Syrjanen A, Reijonen TM, Korhonen K, Korppi M. Wheez-
ing requiring hospitalization in early childhood: predictive factors for
asthma in a six-year follow-up. Pediatr Allergy Immunol 2002; 13:
50. Matthews CE, Ockene IS, Freedson PS, Rosal MC, Merriam PA,
Hebert JR. Moderate to vigorous physical activity and risk of upper-
respiratory tract infection. Med Sci Sports Exerc 2002; 34: 1242-
51. Hemila H, Virtamo J, Albanes D, Kaprio J. Physical activity and the
common cold in men administered vitamin E and beta-carotene.
Med Sci Sports Exerc 2003; 35: 1815-1820.
52. Schouten WJ, Verschuur R, Kemper HC. Physical activity and up-
per respiratory tract infections in a normal population of young men
and women: the Amsterdam Growth and Health Study. Int J Sports
Med 1988; 9: 451-455.
53. Nieman DC. Upper respiratory tract infections and exercise. Thorax
1995; 50: 1229-1231.
54. Alaranta A, Alaranta H, Heliovaara M, Alha P, Palmu P, Helenius I.
Allergic rhinitis and pharmacological management in elite athletes.
Med Sci Sports Exerc 2005; 37: 707-711.
55. Nieman DC, Pedersen BK. Exercise and immune function. Recent
developments. Sports Med 1999; 27: 73-80.
56. Krause R, Patruta S, Daxbock F, Fladerer P, Biegelmayer C, Wenisch
C. Effect of vitamin C on neutrophil function after high-intensity ex-
ercise. Eur J Clin Invest 2001; 31: 258-263.
57. Nieman DC, Peters EM, Henson DA, Nevines EI, Thompson MM.
Inﬂuence of vitamin C supplementation on cytokine changes fol-
lowing an ultramarathon. J Interferon Cytokine Res 2000; 20: 1029-
58. Peters-Futre EM. Vitamin C, neutrophil function, and upper respira-
tory tract infection risk in distance runners: the missing link. Exerc
Immunol Rev 1997; 3: 32-52.
59. Pyne DB, Gleeson M. Effects of intensive exercise training on im-
munity in athletes. Int J Sports Med 1998; 19 Suppl 3: S183-S191.
60. Malm C. Exercise immunology: the current state of man and mouse.
Sports Med 2004; 34: 555-566.
61. MacKinnon LT. Special feature for the Olympics: effects of exercise
on the immune system: overtraining effects on immunity and per-
formance in athletes. Immunol Cell Biol 2000; 78: 502-509.
62. Pedersen BK. Special feature for the Olympics: effects of exercise
on the immune system: exercise and cytokines. Immunol Cell Biol
2000; 78: 532-535.
63. Gleeson M, Pyne DB, Callister R. The missing links in exercise
effects on mucosal immunity. Exerc Immunol Rev 2004; 10: 107-
Current Allergy & Clinical Immunology, June 2010 Vol 23, No. 2 57
64. Jeurissen A, Bossuyt X, Ceuppens JL, Hespel P. [The effects of
physical exercise on the immune system]. Ned Tijdschr Geneeskd
2003; 147: 1347-1351.
65. MacKinnon LT. Chronic exercise training effects on immune func-
tion. Med Sci Sports Exerc 2000; 32(7 Suppl): S369-S376.
66. Gleeson M. Immune function in sport and exercise. J Appl Physiol
2007; 103: 693-699.
67. Green KJ. Improving understanding of exercise effects on in vitro
T-lymphocyte function - the role of ﬂuorescent cell division tracking.
Exerc Immunol Rev 2002; 8: 101-115.
68. McKune AJ, Smith LL, Semple SJ, Wadee AA. Inﬂuence of ultra-
endurance exercise on immunoglobulin isotypes and subclasses.
Br J Sports Med 2005; 39: 665-670.
69. Muns G. Effect of long-distance running on polymorphonuclear neu-
trophil phagocytic function of the upper airways. Int J Sports Med
1994; 15: 96-99.
70. Pedersen BK, Toft AD. Effects of exercise on lymphocytes and cy-
tokines. Br J Sports Med 2000; 34: 246-251.
71. Shephard RJ. Cytokine responses to physical activity, with particular
reference to IL-6: sources, actions, and clinical implications. Crit Rev
Immunol 2002; 22: 165-182.
72. Shinkai S, Kurokawa Y, Hino S, et al. Triathlon competition induced
a transient immunosuppressive change in the peripheral blood of
athletes. J Sports Med Phys Fitness 1993; 33: 70-78.
73. Akimoto T, Kumai Y, Akama T, et al. Effects of 12 months of exer-
cise training on salivary secretory IgA levels in elderly subjects. Br J
Sports Med 2003; 37: 76-79.
74. Ciloglu F. The effect of exercise on salivary IgA levels and the in-
cidence of upper respiratory tract infections in postmenopausal
women. Kulak Burun Bogaz Ihtis Derg 2005; 15(5-6): 112-116.
75. Fahlman MM, Engels HJ, Morgan AL, Kolokouri I. Mucosal IgA
response to repeated wingate tests in females. Int J Sports Med
2001; 22: 127-131.
76. Gleeson M. Mucosal immune responses and risk of respiratory ill-
ness in elite athletes. Exerc Immunol Rev 2000; 6: 5-42.
77. Libicz S, Mercier B, Bigou N, Le Gallais D, Castex F. Salivary IgA
response of triathletes participating in the French Iron Tour. Int J
Sports Med 2006; 27: 389-394.
78. Muns G, Singer P, Wolf F, Rubinstein I. Impaired nasal mucociliary
clearance in long-distance runners. Int J Sports Med 1995; 16: 209-
79. Nehlsen-Cannarella SL, Nieman DC, Fagoaga OR, et al. Saliva im-
munoglobulins in elite women rowers. Eur J Appl Physiol 2000; 81:
80. Reid MR, Drummond PD, MacKinnon LT. The effect of moderate
aerobic exercise and relaxation on secretory immunoglobulin A. Int
J Sports Med 2001; 22: 132-137.
81. Sari-Sarraf V, Reilly T, Doran DA. Salivary IgA Response to Intermit-
tent and Continuous Exercise. Int J Sports Med 2006; 27:849-855.
82. Dressendorfer RH, Petersen SR, Moss Lovshin SE, Hannon JL, Lee
SF, Bell GJ. Performance enhancement with maintenance of rest-
ing immune status after intensiﬁed cycle training. Clin J Sport Med
2002; 12: 301-307.
83. Moreira A, Kekkonen RA, Delgado L, Fonseca J, Korpela R, Haahtela
T. Nutritional modulation of exercise-induced immunodepression in
athletes: a systematic review and meta-analysis. Eur J Clin Nutr
2007; 61: 443-460.
84. Nieman DC. Immunonutrition support for athletes. Nutr Rev 2008;
85. Krieger JW, Crowe M, Blank SE. Chronic glutamine supplementa-
tion increases nasal but not salivary IgA during 9 days of interval
training. J Appl Physiol 2004; 97: 585-591.
86. Nieman DC. Exercise immunology: nutritional countermeasures.
Can J Appl Physiol 2001; 26 Suppl: S45-S55.
87. Nieman DC, Bishop NC. Nutritional strategies to counter stress to
the immune system in athletes, with special reference to football.
J Sports Sci 2006; 24: 763-772.
88. Peters EM. Nutritional aspects in ultra-endurance exercise. Curr
Opin Clin Nutr Metab Care 2003; 6: 427-434.
89. Venkatraman JT, Pendergast DR. Effect of dietary intake on im-
mune function in athletes. Sports Med 2002; 32: 323-337.
90. Cox AJ, Pyne DB, Saunders PU, Fricker PA. Oral administration
of the probiotic Lactobacillus fermentum VRI-003 and mucosal
immunity in endurance athletes. Br J Sports Med 2010; 44: 222-
91. West NP, Pyne DB, Peake JM, Cripps AW. Probiotics, immunity
and exercise: a review. Exerc Immunol Rev 2009; 15: 107-126.
92. Komarow HD, Postolache TT. Seasonal allergy and seasonal dec-
rements in athletic performance. Clin Sports Med 2005; 24(2):
93. MacKnight JM, Mistry DJ. Allergic disorders in the athlete. Clin
Sports Med 2005; 24(3):507-viii.
94. Katelaris CH. Atmospheric emissions and the allergic athlete. In-
ternational Sportmed Journal 2000; 1(2):1-7.
95. Terrell TT, Hough DO, Alexander R. Identifying exercise allergies,
exercise-induced anaphylaxis and cholinergic urticaria. Phys Sports
Med 1996; 24: 76-89.
96. Helenius IJ, Tikkanen HO, Sarna S, Haahtela T. Asthma and in-
creased bronchial responsiveness in elite athletes: atopy and sport
event as risk factors. J Allergy Clin Immunol 1998; 101: 646-652.
97. Helenius IJ, Tikkanen HO, Haahtela T. Occurrence of exercise in-
duced bronchospasm in elite runners: dependence on atopy and
exposure to cold air and pollen. Br J Sports Med 1998; 32: 125-
98. Katelaris CH, Carrozzi FM, Burke TV. Allergic rhinoconjunctivitis in
elite athletes: optimal management for quality of life and perfor-
mance. Sports Med 2003; 33: 401-406.
99. Schwartz LB, Delgado L, Craig T, et al. Exercise-induced hyper-
sensitivity syndromes in recreational and competitive athletes: a
PRACTALL consensus report (what the general practitioner should
know about sports and allergy). Allergy 2008; 63: 953-961.
100. Katelaris CH. Allergic rhinoconjunctivitis – an overview. Acta Oph-
thalmol Scand Suppl 2000; 230: 66-68.
101. Katelaris CH, Carrozzi FM, Burke TV, Byth K. A springtime olym-
pics demands special consideration for allergic athletes. J Allergy
Clin Immunol 2000; 106: 260-266.
102. Bonsignore MR, Morici G, Vignola AM, et al. Increased airway in-
ﬂammatory cells in endurance athletes: what do they mean? Clin
Exp Allergy 2003; 33: 14-21.
103. Karjalainen EM, Laitinen A, Sue-Chu M, Altraja A, Bjermer L,
Laitinen LA. Evidence of airway inﬂammation and remodeling in
ski athletes with and without bronchial hyperresponsiveness to
methacholine. Am J Respir Crit Care Med 2000; 161: 2086-2091.
104. Leonard EG. Viral myocarditis. Pediatr Infect Dis J 2004; 23: 665-
105. Shephard RJ, Shek PN. Infectious diseases in athletes: new inter-
est for an old problem. J Sports Med Phys Fitness 1994; 34: 11-
106 Roberts JA. Viral illnesses and sports performance. Sports Med
1986; 3: 298-303.
107. Friman G, Wright JE, Ilback NG, et al. Does fever or myalgia in-
dicate reduced physical performance capacity in viral infections?
Acta Med Scand 1985; 217: 353-361.
108. Friman G. Effect of acute infectious disease on isometric muscle
strength. Scand J Clin Lab Invest 1977; 37: 303-308.
109. Friman G. Effects of acute infectious disease on circulatory func-
tion. Acta Med Scand Suppl 1976; 592: 1-62.