monitoring stress tolerance and occurrences of upper respiratory illness in basketball players by...
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e166 Stress and Health 27: e166–e172 (2011) © 2010 John Wiley & Sons, Ltd.
RESEARCH ARTICLE
Monitoring Stress Tolerance and Occurrences of Upper Respiratory Illness in Basketball Players by Means of Psychometric Tools and Salivary BiomarkersAlexandre Moreira1*†, Franco Arsati2, Ynara Bosco de Oliveira Lima-Arsati2, Antonio Carlos Simões1 & Vera Cavalcanti de Araújo3
1Department of Sport, School of Physical Education and Sport, University of São Paulo, São Paulo, Brazil2Department of Physiological Sciences, São Leopoldo Mandic Dental Research Center, Campinas, Brazil3Department of Oral Pathology, São Leopoldo Mandic Dental Research Center, Campinas, Brazil
Abstract
The aim of the study was to evaluate the possible relationships between stress tolerance, training load, banal infec-
tions and salivary parameters during 4 weeks of regular training in fi fteen basketball players. The Daily Analysis of
Life Demands for Athletes’ questionnaire (sources and symptoms of stress) and the Wisconsin Upper Respiratory
Symptom Survey were used on a weekly basis. Salivary cortisol and salivary immunoglobulin A (SIgA) were col-
lected at the beginning (before) and after the study, and measured by enzyme-linked immunosorbent assay (ELISA).
Ratings of perceived exertion (training load) were also obtained. The results from ANOVA with repeated measures
showed greater training loads, number of upper respiratory tract infection episodes and negative sensation to both
symptoms and sources of stress, at week 2 (p < 0.05). Signifi cant increases in cortisol levels and decreases in SIgA
secretion rate were noted (before to after). Negative sensations to symptoms of stress at week 4 were inversely and
signifi cantly correlated with SIgA secretion rate. A positive and signifi cant relationship between sources and symp-
toms of stress at week 4 and cortisol levels were verifi ed. In summary, an approach incorporating in conjunction
psychometric tools and salivary biomarkers could be an effi cient means of monitoring reaction to stress in sport.
Copyright © 2010 John Wiley & Sons, Ltd.
Received 29 March 2010; Accepted 13 August 2010; Revised 13 June 2010
Keywords
salivary immunoglobulin A; salivary cortisol; sports; immune function; hypothalamic-pituitary-adrenal axis; psychological stress
*Correspondence
Alexandre Moreira, Av. Prof. Mello de Moraes, 65—Cidade Universitária, CEP 05508-030, São Paulo, SP, Brazil.†Email: [email protected]
Published online 5 October in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/smi.1354
Introduction
An accumulation of stress in athletes must be consid-
ered in both a sport and a non-sport environment. The
necessity of utilizing markers to monitor these reac-
tions in a practical setting is evident. Even recognizing
that the physiological stress could be considered as the
most important cause of distinct syndromes as non-
functional overreaching and overtraining (Nederhof,
Lemmink, Visscher, Meeusen, & Mulder, 2006), early
insights pointed toward the combination with the
psychological and/or social stressors in relation to
regeneration (Hooper & Mackinnon, 1995; Kentta &
Hassmen, 1998; Lehmann, Foster, & Keul, 1993).
Budgett (1990) suggested that only a small increase
in the total stress (considering the stressors with dis-
tinct categories), in addition to the physiological stress
(by training), might induce what the author named
Stress and Health 27: e166–e172 (2011) © 2010 John Wiley & Sons, Ltd. e167
A. Moreira et al. Monitoring Stress in Basketball Players
‘staleness’ that is a term also used for the ‘overtraining
syndrome’ or just ‘overtraining’, especially in the Euro-
pean literature (Nederhof et al., 2006).
Salivary cortisol, as a representative of circulating
free cortisol has been recommended as an index of
training stress (Passelergue & Lac, 1999) and its use has
also been adopted because this avoids the stress caused
by venepuncture (Lac, Lac, & Robert, 1993) and refl ects
the free plasma concentration and bioactive compo-
nent of steroid hormones. In addition, salivary cortisol
levels parallel those in plasma following adrenocorti-
cotropic hormone and corticotropin-releasing horm-
one stimulation, and following exercise induced-stress
(Gozansky, Lynn, Laudenslager, & Kohrt, 2005; Vining,
McGinley, Maksvytis, & Ho, 1983). Vining et al. (1983)
also suggested that salivary cortisol may actually provide
a better measure of the stress response than serum cor-
tisol as it more accurately measures the amount of
unbound cortisol compared to serum measurements.
It has also been proposed that an increased secretion
of glucocorticoids could induce depression of immune
cell functions (Fleshner, 2000). Wira, Sandoe, and
Steele (1990) demonstrated that the potent synthetic
glucocorticoid dexamethasone causes a decline in the
salivary immunoglobulin A (SIgA) concentration 24 h
after a single injection. SIgA is the most commonly
studied marker of the mucosal immune system (Bishop
& Gleeson, 2009).
The athletes’ vulnerability to respiratory tract infec-
tions is one of the features of most interest to researchers
of different disciplines. Recently, Martin, Pence, and
Woods (2009) provided evidence to support the
increased susceptibility to upper respiratory tract infec-
tions (URTI) with chronic stressors with their research
in mice, which is consistent with the observational data
regarding exercise and illness incidence in humans. For
example, Neville, Gleeson, and Folland (2008) recently
showed a signifi cant reduction (28%) in SIgA occurring
during the 3 weeks before URTI episodes and returned
to baseline 2 weeks after an URTI. When an athlete did
not have, or was not recovering from URTI, a SIgA value
lower than 40% of their mean healthy SIgA concentra-
tion indicated a 50% chance of contracting an URTI
within 3 weeks. In addition, the authors affi rm that the
relationship between physiological and psychological
stress and immune function is widely recognized.
The necessity of monitoring URTI episodes that
could be associated to stress tolerance and might impair
performance by means of simple tools is evident. Unfor-
tunately, there is relatively little research with valid,
practical and noninvasive tools to monitor stress state
and URTI episodes with elite young team players. Mon-
itoring changes in sources and symptoms of stress in
team-sports, including its relationship with banal infec-
tions, particularly URTI, may assist coaches to control
appropriately the training process. In addition, the link
between salivary cortisol and SIgA levels with URTI
episodes and stress tolerance needs to be elucidated.
Therefore, the aim of the present study was to evalu-
ate if sources and symptoms of stress as well as the
occurrence of URTIs could be associated with changes
in salivary cortisol and SIgA during a competitive train-
ing period in elite young basketball players. It was
hypothesized that there would be a relationship between
stress tolerance, training load, banal infections and sali-
vary parameters during the investigated training period.
Material and methods
Participants
The sample comprised 15 male basketball players
([mean and standard deviation to age = 19 ± 0.6 years,
height 192 ± 10 cm, body mass 92 ± 9 kg). They com-
menced the observation period in a good health state,
as assessed by a medical screening. None of them were
receiving medication or had suffered from a debilitat-
ing infection in the preceding 2 weeks. They usually
trained for 90–120 min per session, two sessions per
day, and fi ve days per week. The investigated team was
successful reached the second position at the Under-19
State Championship. The investigated athletes also
usually train and/or compete with the main (adult)
team. Their habitual training sessions consisted of one
tactical and technical session, one specifi c conditioning
work as well as weight training and plyometric training.
After being informed of the experimental procedures,
including potential benefi ts and risks, the athletes gave
written consent to participate. The local ethics commit-
tee approval was previously obtained.
Experimental design
The study observations were carried out over a 4-week
period during the competitive season. After these four
investigated weeks, the team was involved in the play-
off matches from the State Championship. Therefore,
the last investigated week could be considered as a
‘taper’ week, with a reduction in both training time and
Monitoring Stress in Basketball Players A. Moreira et al.
e168 Stress and Health 27: e166–e172 (2011) © 2010 John Wiley & Sons, Ltd.
training intensity. During the experimental period, they
played one game per week. Ratings of perceived exer-
tion (session-RPE) after each exercise session in each
day throughout 28 days were obtained from all athletes
involved in the study. A Daily Analysis of Life Demands
for Athletes’ questionnaire (DALDA; sources and symp-
toms of stress) and the Wisconsin Upper Respiratory
Symptom survey (WURSS-21) to monitor the symp-
tomatology of URTI were used on a weekly basis. Saliva
samples were collected at the beginning of the study
and one week after the fi nish of the experiment. The
saliva samples were collected at rest, in the afternoon,
at the same time of day both before and after the inves-
tigated period. The recovery interval from the last bout
of exercise was at least 10–12 h. The subjects abstained
from food and caffeine products for 60–90 min prior
to the saliva collection.
Saliva collection
The subjects were in a seated position, with eyes open,
head tilted slightly forward and making minimal oro-
facial movement. Unstimulated saliva was collected
into sterile 15-mL centrifuge tubes over a 5-min period.
Immediately after collection, the saliva samples were
frozen and stored at −80°C until assayed for cortisol
and SIgA concentration.
Assays
Salivary immunoglobulin A concentration was mea-
sured by enzyme linked immunosorbent assay (ELISA,
SIgA EIA kit, ALPCO Diagnostics, Salem, MA, USA) in
accordance with our previous work (Moreira, Arsati,
Cury, et al., 2009; Moreira et al., 2008). The SIgA secre-
tion rate (SIgArate; μg·min−1) was calculated by multi-
plying the absolute SIgA concentration by salivary fl ow
rate (mL·min−1). Salivary fl ow rate was determined by
dividing the volume of saliva collected by the duration
of the sampling period. The cortisol concentration was
also measured by enzyme-linked immunosorbent assay
(ELISA, Cortisol—Direct Salivary EIA; ALPCO Diag-
nostics, Salem, MA, USA) in accordance with our pre-
vious work (Moreira, Arsati, de Oliveira Lima Arsati, da
Silva, & de Araújo, 2009).
Monitoring training load
The training load (TL) for each athlete during each
training session was calculated according to the methods
of Foster (Foster, 1998). This method of monitoring TL
requires each athlete to provide an RPE (CR-10 scale)
for each exercise session along with a measure of train-
ing time. To approach the session intensity, athletes
were asked after 30 min of the end of their workout a
simple question: ‘How was your workout?’ A single
number representing the magnitude of TL for each
session was then calculated by the multiplication of
training intensity by its duration (TL = Session-RPE ×
duration in min).
DALDA
DALDA (Rushall, 1990) was also completed on days 7,
14, 21 and 28 by each athlete. The DALDA is divided
into two parts, namely Part A and Part B, which repre-
sent the sources of life stress and symptoms of stress,
respectively. The athletes were asked rate each item to
‘worse than normal’, ‘normal’ or ‘better than normal’.
The responses ‘worse than normal’ were retained for
analysis. Although it is advised that the DALDA be used
on a daily basis or every other day, it was previously used
on a weekly basis without having its sensitivity dimin-
ished (Robson-Ansley, Blannin, & Gleeson, 2007).
Upper respiratory illness questionnaire
A short version of the WURSS-44, the WURSS-21
(Barrett et al., 2005) was utilized to measure all signifi -
cant health-related dimensions that are negatively
affected to the common cold. It was assumed that the
responses by WURSS-21 would be a reasonable marker
of symptomatology of URTI and functional impair-
ment according to previous studies (Spence et al.,
2005). The WURSS-21 includes 10 items assessing
symptoms, nine items assessing functional impair-
ments and 1 item each assessing global severity and
global change (‘How sick do you feel today?’ and ‘com-
pared to yesterday, I feel that my cold is . . .’). All the
items are responded using a Likert scale of severity,
ranging from 0–7. The total number of occurrences
regardless of severity level was retained for analysis.
Statistical analyses
Data is reported as means and standard error of
the mean (SEM). The distribution of the data was
analyzed by the Shapiro-Wilk test. The Mauchly’s
Test of Sphericity was performed to test the null
hypothesis that the error covariance matrix of the
Stress and Health 27: e166–e172 (2011) © 2010 John Wiley & Sons, Ltd. e169
A. Moreira et al. Monitoring Stress in Basketball Players
orthonormalized-transformed dependent variables was
proportional to an identity matrix. An ANOVA with
repeated measures was used to compare the four
moments (week 1, 2, 3 and 4) for each dependent vari-
able. Salivary cortisol and SIgA levels were compared
between week 1 and week 4. Tukey HSD post hoc test
was utilized when necessary. In the case of violation of
the assumption of sphericity, the signifi cance was estab-
lished by utilizing the Greenhouse-Geisser correction.
The relationships between dependent variables were
evaluated by means of Pearson product moment cor-
relation. The level of signifi cance was set at 0.05.
Results
Table I shows the weekly training load measured during
the experimental training period. A signifi cant differ-
ence between the second and the fourth week was
observed (p < 0.05). The values refl ect an average
weekly training load (accumulated diary training load
divided by number of the sessions in each week).
In Table II, the values from absolute SIgA concen-
tration (SIgAabs), SIgA secretion rate (SIgArate) and
salivary cortisol before commencement of the training
and 1 week after the training period are revealed. The
signifi cant increases in cortisol levels and decreases in
SIgArate were verifi ed (p < 0.05; before to after
moments).
Figure 1 illustrates the dynamics of the symptom-
atology of URTI. Signifi cant differences (p < 0.05)
between week 2 to weeks 1 and 4 were verifi ed, reveal-
ing the great number of episodes in week 2.
In Figure 2, the number of responses ‘worse than
normal’ from part A of DALDA, indicates the dynamics
of sources of stress. Signifi cant differences were observed
from week 2 to week 1, 3 and 4 (p < 0.05).
In Figure 3, the number of responses ‘worse than
normal’ from part B of DALDA, indicates the dynamics
Table I. Weekly training load measured during the study period; mean (SEM)
Week 1 Week 2 Week 3 Week 4
Training load 656 (92) 680 (83) 548 (37) 479 (34)*
Training load [Arbitrary units (AU)].
* Signifi cant difference from week 2 (p < 0.05).
Table II. Mean and SEM of SIgAabs, SIgArate and salivary cortisol before and after the investigated training period
Before training
period
After training
period
Salivary cortisol (ng·ml−1) 17.6 (1.8) 26.8 (4.9)*
SIgAabs (μg·mL−1) 587 (94) 720 (153)
SIgArate (μg·min−1) 106 (20) 92 (21)*
Before training period: before commencement of the investigated
training period; after training period: 1 week after the investigated
training period; SIgAabs: absolute SIgA concentration; SIgArate: SIgA
secretion rate.
* Signifi cant difference between before and after training period
(p < 0.05).
Figure 1 Total number of occurrences (symptomatology of upper
respiratory tract illness—responses from WURSS-21). *Signifi cant
difference from week 2 (p < 0.05)
Figure 2 Numbers of responses ‘worse than normal’—Sources of
stress (Part A of DALDA). *Signifi cant difference from week 2
(p < 0.05)
Figure 3 Numbers of responses ‘worse than normal’ Symptoms
of stress (Part B of DALDA). *Signifi cant difference from week 2
(p < 0.05)
Monitoring Stress in Basketball Players A. Moreira et al.
e170 Stress and Health 27: e166–e172 (2011) © 2010 John Wiley & Sons, Ltd.
of symptoms of stress. Signifi cant differences (p < 0.05)
were observed between week 2 and week 4.
In Table III, only the signifi cant correlations between
dependent variables are presented.
Discussion
The results from the present study showed an interest-
ing perspective to use the DALDA and WURSS-21
questionnaires together with training load to monitor
training. Signifi cant differences between week 2 and
other weeks in sources and symptoms of stress
(DALDA) and URTI symptomatology (WURSS-21)
were revealed.
These results corroborate the assumption of differ-
ent authors considering the importance of monitoring
perceived stress. For example, Kentta and Hassmen
(1998) proposed the onset of staleness is caused by an
increase in psychological and/or social stress, leading to
an inability to recover from a previous physiological
stress. It is important to note that in the present study,
the greater negative responses, represented by the rise
in total occurrences (episodes) of URTI, emerged
during the second week; during this same week, partici-
pants reported the greatest number of responses ‘worse
than normal’ in sources and symptoms of stress dem-
onstrating that social and psychological stress factors in
conjunction with physiological stress (training load)
have a considerable role to the adaptation process.
Indeed, our results are in agreement with the fi nd-
ings from Main and Grove (2009) who reported the
initial validation of a multi-component assessment
model for monitor training distress among athletes.
Moreover, recent developments suggest that the brain
and the peripheral immune system cells form a bidirec-
tional communication network (Quan & Banks, 2007).
Fry, Morton and Keast (1991) proposed some ‘cat-
egories’ with the aim to monitoring training, which
include physiological and psychological dimensions as
well as the biochemical and immunological aspects.
The agreement concerning the data from the question-
naires utilized in the present study reinforces the notion
that the training load in conjunction with the social and
psychological aspects needs to be considered. Indeed,
our results are in accordance with the practical methods
of monitoring and managing fatigue in athletes explored
and proposed recently (Robson-Ansley, Gleeson, &
Ansley, 2009).
In respect of hormonal and mucosal immune param-
eters, the results showed that salivary cortisol levels rose
from before to after investigated training period despite
the signifi cant reduction in training load from the
second to the fourth week. So, it is plausible that not
only the training load but also the psychological factor
were crucial to this alteration. Additionally, it is reason-
able to speculate that these changes in salivary cortisol,
could be linked, at least in part, with the reduction in
SIgArate from before to after moment, considering that
the stress hormone is potent modulators of immune
function.
An inherent drawback of the current study is the
inability to monitor the salivary parameters during all
the investigated weeks, yet they were measured only at
the beginning and end of the training period. All the
other variables were measured each week. Correlations
would have been done over the four time points. Nev-
ertheless, despite of these limitations, the present fi nd-
ings revealed some interesting fi ndings about the
possible association among the investigated psycho-
metrics tolls, hormonal and mucosal immune param-
eters in team-sports, as well as the usefulness of this
approach to monitor training.
Table III. Signifi cant correlations between dependent variables (p < 0.05)
Pearson correlations (r) Symptomatology of
URTI—week 2 (WURSS-21)
Before—Salivary cortisol After—Salivary cortisol Before—SIgArate
Sources of stress week 2
(DALDA—Part A)
0.79
Symptoms of stress week 2
(DALDA—Part B)
0.65
Symptoms of stress week 4
(DALDA—Part B)
0.67 0.75 −0.73
Before: before commencement of the investigated training period; After: 1 week after the investigated training period.
DALDA: The Daily Analysis of Life Demands for Athletes’ questionnaire; SIgArate: SIgA secretion rate; URTI: upper respiratory tract infection;
WURSS-21: Wisconsin Upper Respiratory Symptom Survey.
Stress and Health 27: e166–e172 (2011) © 2010 John Wiley & Sons, Ltd. e171
A. Moreira et al. Monitoring Stress in Basketball Players
Multiple stressors are likely to induce changes in
mucosal immunity. For example, psychological stress
source is thought to infl uence mucosal immune func-
tion (Jemmott et al., 1983). This possible link between
stress markers and mucosal immunity are reinforced
in the present study, by the fact that the initial levels
of SIgArate were negatively and signifi cantly corre-
lated with the signs and symptoms of stress at the
fourth week, what could indicate that the athletes with
low initial levels of SIgArate (low protection against
pathogens) are more susceptible to be affected by dif-
ferent stressors. In addition, the positive relationship
between symptoms of stress at week four and cortisol
concentrations from both before and after moments,
suggests that a link might exist between these markers.
Further studies taken account the investigated markers
used in the present study, with a longitudinal approach
during the competition season should be considered.
In summary, the present study showed an interesting
congruence between DALDA, WURSS-21 and session-
RPE responses revealing the usefulness of these instru-
ments in a practical setting. The positive relationship
between salivary cortisol levels and sources and symp-
toms of stress showed an agreement between stress mea-
sured by this psychometric instrument and the stress
hormone response. The necessity of monitoring banal
illness that could be associated to stress tolerance and
might impair performance was successfully approached
by the WURSS-21 questionnaire. Moreover, the fi nd-
ings suggest that the athletes with low initial levels of
SIgArate are more susceptible to be affected by different
stressors. A systematic approach incorporating in con-
junction some features linked to training load, per-
ceived stress and indicators of upper respiratory tract
illness could be an effi cient means of monitoring both
stress and recovery in a holistic way and within the
perspective of a biopsychosocial stress model.
Acknowledgments
We would like to thank the FAPESP—São Paulo
Research Foundation (process, 2008/10404-3) for
funding this research. We also wish to acknowledge all
basketball players and research support staff (particu-
larly, Murilo Drago and Gustavo Drago) involved in
this study for their committed participation.
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