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Premenstrual Syndrome, Inflammatory Status, and Mood States in Soccer

Players

Article  in  NeuroImmunoModulation · January 2019

DOI: 10.1159/000494559

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 Original Paper

Neuroimmunomodulation Received: May 22, 2018

Accepted after revision: October 13, 2018
DOI: 10.1159/000494559 Published online: January 17, 2019

Premenstrual Syndrome, Inflammatory

Status, and Mood States in Soccer Players
Roberta Foster a Mauro Vaisberg b André Luis Lacerda Bachi c
     

Juliana de Melo Batista dos Santos b Rodolfo de Paula Vieira c, d

   

Luiz Antonio Luna-Junior b Maita Poli Araújo a Tathiana Rebizzi Parmigiano a

     

Fernanda Borges e Zsuzsanna I.K.J. Di-Bella a
   

a Department of Gynecology, Federal University of São Paulo, São Paulo, Brazil; b Department of
   

Otorhinolaryngology and Head and Neck Surgery, Federal University of São Paulo, São Paulo, Brazil;
c Brazilian Institute of Teaching and Research in Pulmonary and Exercise Immunology (IBEPIPE),
 

São José dos Campos, Brazil; d Postgraduate Program in Sciences of Human Movement and Rehabilitation,
 

Federal University of São Paulo, Campus Baixada Santista, Santos, Brazil; e Nephrology Division of
 

the Medicine Department, Federal University of São Paulo, São Paulo, Brazil

Keywords
Female soccer players · Premenstrual syndrome ·
Inflammation · Mood states · Stress hormones
Abstract
Objective: To evaluate the relationship between the inflam-
matory profile and mood states in the different phases of the
menstrual cycle in soccer players with and without premen-
strual syndrome (PMS). Methods: Data on the menstrual cy-
cle and mood states were collected using the Daily Symptom
Report and the Brunel Mood Scale. Cytokine and stress hor-
mone concentrations were measured in urine by flow cy-
tometry before and after a game in the luteal phase and in
the follicular phase of one menstrual cycle. Results: In all,
59.6% of the athletes had PMS. The PMS group showed high-
er concentrations of interleukin (IL)-1β, IL-6, and IL-8 than
the athletes without PMS. After the game, IL-6 decreased in
the follicular phase and the luteal phase. The tumor necrosis
factor-α levels were higher in the group without PMS during
the post-game follicular phase than before the game. In the
PMS group, tension was higher in the follicular phase before
the game and depression was higher in the pre-game luteal
phase than in the group without PMS. The PMS group also
presented a negative correlation between depression and
IL-10 levels in the pre-game follicular phase. Finally, in the
pre-game luteal phase were found positive correlations be-
tween growth hormone and IL-10. Conclusion: PMS influ-
ences the inflammatory condition related to mood states
and stress hormones in female soccer players.
© 2019 S. Karger AG, Basel
Introduction
Premenstrual syndrome (PMS) is a functional and re-
current syndrome characterized by physical symptoms
and psychological disturbances [1]. The prevalence of
161.116.100.134 - 1/18/2019 11:48:26 AM

© 2019 S. Karger AG, Basel Dr. Mauro Vaisberg

Federal University of Sao Paulo, Department of Otorhinolaryngology and
Universitat de Barcelona

Head and Neck Surgery, Rua Napoleão dos Otonis, 700

E-Mail karger@karger.com
Vila Clementino, São Paulo, SP 04025-002 (Brazil)
www.karger.com/nim
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E-Mail vaisberg.mauro @ gmail.com

PMS ranges from 8 to 86%, with differences in intensity
and type of symptoms [2, 3]. Despite the fact that physical
exercise improves the symptomatology of PMS [4], the
effects of PMS on athletes have been poorly studied [4].
Therefore, studies on athletes with PMS could improve
our understanding of the influences of PMS on several
aspects related to the performance of these athletes [5].
Beyond their action on the immune system, cytokines
also have an important role during the reproductive cycle
[6], besides being important regulators of organic ho-
meostasis during physical exercise. Interleukin (IL)-1β
and tumor necrosis factor (TNF)-α are the main pro­
inflammatory cytokines, being produced by immune and
muscle cells [7]. IL-6 is the main cytokine studied in the
context of physical exercise. Its gene is silenced at rest but
is rapidly transcribed during physical exercise via muscle
contraction, leading to an increase in intra- and extracel-
lular concentrations of this cytokine [8]. During strenu-
ous and prolonged exercise, it also promotes the release
of stress hormones such as cortisol into the circulation
[9]. IL-8 belongs to the chemokine family and acts by pro-
moting the migration of monocytes and neutrophils to
sites of inflammation through the expression of adhesion
molecules that facilitate the infiltration process into the
injured tissue. IL-10 classically has an anti-inflammatory
role in response to exercise, but it also acts on the brain
and on behavior [10].
Despite the important influence of cytokines during
the reproductive cycle, there have been few studies evalu-
ating the possible actions of cytokines during PMS. Ber-
tone-Johnson et al. [11] demonstrated that inflammatory
markers were increased in women with PMS, especially
in those with exacerbated symptoms.
Athletes in precompetitive periods may present emo-
tional changes that compromise their physical abilities,
leading to altered performance. A good performance de-
pends on a good emotional balance, so it is important to
evaluate behavioral changes such as mood states in ath-
letes [12–14]. The objective of this study was to evaluate
the relationship between the inflammatory profile and
mood states in the different phases of the menstrual cycle
in a group of soccer players with and without PMS.
Subjects and Methods
A previous study published by Foster et al. [12] evaluated 52
female soccer players (aged 19.8 ± 4.7 years) who had played pro-
fessionally in championships in 2012 in São Paulo and determined,
with the Daily Symptom Report (DSR), the presence of PMS in 31
players (59.6%) and its absence in 21 players (40.4%). Kindly, this
2 Neuroimmunomodulation
DOI: 10.1159/000494559
Table 1. Analysis of urinary cytokine concentrations in female soc-
cer players with PMS and without PMS
Cytokine Without PMS With PMS p
(n = 21) (n = 31)
IL-1β 0.90±0.25 1.12±0.23 0.01
IL-6 6.45±1.01 9.48±1.68 0.001
IL-8 0.81±0.10 1.26±0.48 0.04
IL-10 0.98±0.12 0.97±0.09 0.74
TNF-α 1.15±0.23 1.23±0.36 0.58
All parameters are expressed as mean square root osm (pg/
mL) ± standard deviation. PMS, premenstrual syndrome.
group of volunteers took part in the continuation of our study.
This way, the collected urine samples could be used for new analy-
ses and other questionnaires were evaluated.
The calculation of the sample size, the inclusion and exclusion
criteria of the study, the number of protocols and consent forms,
and the training schedules, as well as the methods of PMS assess-
ment, urine sample collection, and urine osmolality determination
were presented in our previous study [12].
Anthropometric data (weight and height) were collected from
all volunteers via clinical measurement performed by a qualified
professional and using a mechanical anthropometric scale (Filizo-
la®). The BMI was calculated from weight and height by the for-
mula weight (kg)/height (m)2. The age of the volunteers was veri-
fied via their personal identification documents.
Cytokine and Hormone Measurements
The cytokines IL-1β, IL-6, IL-8, IL-10, and TNF-α, as well as
growth hormone, were assessed using the HCYTOMAG-60K kit
and read and analyzed with a flow cytometer (Luminex xMAP;
EMD Millipore, Billerica, MA, USA) as demonstrated in our previ-
ous study. All samples collected were thawed at the same time and
were measured together.
Urine was used to assess the cytokines and the hormone. The
values obtained from urine were normalized through urine osmo-
lality, since the urine may be more concentrated or diluted accord-
ing to the loss of fluid as well as the hydration of the athletes.
Urinary creatinine was measured to rule out the possibility of
altered renal function. Urine creatinine concentrations were deter-
mined using a colorimetric kinetic kit (Siemens Healthcare Diag-
nostics Inc., Newark, DE, USA) and the results were analyzed with
an automated system (Dimension RxL Max Integrated Chemistry
System; Siemens Healthcare Diagnostics Inc.).
Evaluation of Mood States
The Brunel Mood Scale (BRUMS), abbreviated and validated
for the Brazilian population by Rohlfs et al. [15], was used to de-
termine the mood states of the volunteers at the four moments
evaluated. The questionnaire has 24 simple adjectives linked to 6
mood subscales: tension, depression, anger, vigor, fatigue, and
confusion. Each subscale consists of 4 “scores”: (a) tension: anx-
ious, worried, nervous, and panicky; (b) depression: depressed,
downhearted, discouraged, and unhappy; (c) anger: annoyed, an-
gry, bitter, and bad-tempered; (d) vigor: lively, energetic, active,
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Foster et al.
Universitat de Barcelona
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 Table 2. Analysis of urinary cytokine concentrations in female soccer players with PMS and without PMS before
and after the game in both the follicular and the luteal phase

Cytokine PMS Follicular phase Luteal phase

before game after game before game after game

IL-1β yes 1.48±1.78 1.33±1.24 1.18±1.46 0.94±0.90

no 1.21±1.31 1.01±0.75 0.76±0.57 0.65±0.22
IL-6 yes 11.2±9.52+ 8.25±5.26+ 10.5±9.49* 7.86±4.41*
no 7.64±4.26 6.37±2.74 6.63±4.13 5.18±2.84
IL-8 yes 1.59±3.58 1.76±3.83 0.81±0.50 0.87±0.65
no 0.85±0.50 0.95±0.72 0.70±0.43 0.77±0.52
IL-10 yes 0.92±0.26 1.11±0.57 0.93±0.30 0.91±0.22
no 1.04±0.33 1.09±0.49 0.82±0.17 0.98±0.39
TNF-α yes 1.40±1.73 1.67±2.38 0.89±0.66 0.98±0.67
no 1.08±0.76# 1.47±1.40# 0.93±0.62 1.14±1.15

All parameters are expressed as mean square root osm (pg/mL) ± standard deviation. PMS, premenstrual
syndrome. + p = 0.02: difference between the values observed before and after the game in the follicular phase in
the PMS group; * p = 0.03: difference between the values observed before and after the game in the luteal phase
in the PMS group; # p = 0.03: difference between the values observed before and after the game in the follicular
phase in the group without PMS.

and alert; (e) fatigue: tired, sleepy, exhausted, and worn out; and
(f) confusion: mixed up, muddled, confused, and uncertain. We
calculated a total score by adding the scores on each subscale,
yielding a total ranging from 0 to 16.
Statistical Analysis
An evaluation of the normality of the data, correction of the
data collected from the urine samples, and the age, weight, height,
and BMI data were presented in our previous study [12].
Student’s t test was used to analyze differences in age, height,
weight, and BMI. ANOVA for repeated measures and Tukey’s
multiple comparison were used to compare the cytokine data be-
tween the group with PMS and the group without PMS at the 4
moments of sampling, and Pearson’s correlation was used to de-
termine the correlations between the markers evaluated. The sig-
nificance level was set at 5% (p < 0.05).
Results
nificant difference in IL-6: in the follicular and luteal
phases there was a decrease after the game (Table 2). The
TNF-α concentration in the group without PMS was
higher during the follicular phase after the game than be-
fore the game (Table 2).
The evaluation of the mood states among the groups
revealed an increase in tension in the pre-game follicular
phase and of depression in the pre-game luteal phase,
both in the PMS group (Table 3). No differences were ob-
served between the groups regarding growth hormone.
The correlation results show a negative correlation be-
tween depression level and IL-10 (ρ = –0.42, p < 0.05) in
the pre-game follicular phase in the PMS group (Fig. 1)
and a positive correlation in the pre-game luteal phase
between growth hormone and IL-10 (ρ = 0.62, p < 0.01)
(Fig. 2).

In the previous study performed with these volunteers, Discussion

no differences were observed in the anthropometric data
between the group with PMS and the group without PMS.
The analysis of urine cytokine concentrations, comparing
only differences between the group with PMS and the
group without PMS, revealed significant alterations in the
cytokines IL-1β, IL-6, and IL-8, showing an increase in
the group with PMS (Table 1). In addition, the analysis of
the 4 moments evaluated (before and after the game in
both the follicular and the luteal phase) revealed a sig-
Our study demonstrated that soccer players with PMS
had an inflammatory status related to PMS. In addition
to this finding, we found correlations between mood
states, cytokines, and stress hormone level. To our knowl-
edge, this is the first study to evaluate the production of
cytokines, mood states, and stress hormone levels in fe-
male soccer players affected and not affected by PMS who
performed an acute exercise in both phases of the men-
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PMS, Inflammation, and Mood States in Neuroimmunomodulation 3

Soccer Players DOI: 10.1159/000494559
Universitat de Barcelona
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 Table 3. Analysis of BRUMS scores of female soccer players with PMS and without PMS before and after the game
in both the follicular and the luteal phase

Brunel mood PMS Follicular phase Luteal phase

state before game after game before game after game

Anger yes 2.74±3.29 2.26±2.87 1.87±2.62 2.16±2.77

no 2.38±3.14 2.24±3.05 1.05±1.69 1.29±2.37
Confusion yes 1.29±1.68 0.81±1.62 0.97±1.43 0.74±1.44
no 0.71±1.10 0.57±0.98 0.29±0.72 0.14±0.36
Depression yes 1.32±2.13 1.55±2.20 1.48±2.19+ 1.32±2.10
no 0.81±1.66 0.76±1.89 0.19±0.68+ 0.48±0.93
Fatigue yes 1.87±2.19 3.55±3.25 2.32±3.33 3.61±3.61
no 2.90±3.34 3.67±3.55 1.67±2.31 2.14±2.45
Tension yes 3.00±2.68# 1.87±2.22 1.93±2.59 1.45±1.93
no 1.7±2.12# 1.33±1.53 1.01±1.30 0.76±1.04
Vigor yes 8.03±3.15 5.42±2.86 5.81±2.93 4.61±3.09
no 6.71±4.04 6.05±3.64 6.62±3.35 3.95±3.31

All parameters are expressed in mean ± standard deviation (SD). PMS, premenstrual syndrome. + p = 0.03:
difference in the values observed before the game between the group with PMS and the group without PMS;
# p = 0.04: difference in the values observed before the game between the group with PMS and the group with-

out PMS.

2.0 2.5

r = –0.42 r = 0.62
IL-10 concentration, pg/mL

IL-10 concentration, pg/mL

p < 0.05 2.0 p < 0.001

1.5

1.5
1.0
1.0

0.5
0.5

0 0
0 2 4 6 8 10 0 10 20 30
Depression score GH concentration, pg/mL

Fig. 1. Correlation between pre-game concentrations of IL-10 and Fig. 2. Correlation between pre-game concentrations of IL-10 and
depression score in the premenstrual syndrome group during the growth hormone (GH) in the premenstrual syndrome group dur-
follicular phase. ing the luteal phase.

strual cycle. One limitation of our study was the use of
urine as the biological sample, which is not common in
cytokine analysis. We chose to evaluate cytokine and
stress hormone levels in urine as it was difficult to collect
blood samples, since the athletes feared this invasive pro-
cedure. Another limitation of the study concerns IL-6. It
was not possible to confirm the origin of the IL-6 concen-
trations observed in the PMS group after the game in the
follicular and luteal phases. However, the results present-
ed are relevant and consistent.
IL-6 is the cytokine most commonly evaluated in
sports studies, due to its modulatory functions of inflam-
matory and metabolic responses to acute exercise, acting
to reduce inflammation and as an “energy sensor” [16].
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4 Neuroimmunomodulation Foster et al.

DOI: 10.1159/000494559
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In this study, we observed an increase in the proinflam-
matory cytokines IL-1β, IL-6, and IL-8 in the PMS group
when compared to the group without PMS. This result
evidences the existence of an inflammatory process, pos-
sibly associated with PMS and not with the exercise per-
formed by the volunteers, since all the athletes evaluated
trained according to the same schedule (including type,
intensity, duration, and rest periods).
The literature shows that IL-6 is a cytokine with pro-
inflammatory action when secreted at rest; thus, the IL-6
found before the game is associated with a proinflamma-
tory profile [17]. On the other hand, physical exercise
leads to an increase in IL-6 produced by skeletal muscle,
with anti-inflammatory actions [18, 19]. Our data showed
a significant decrease in this cytokine in the PMS group
after acute exercise in both phases of the cycle. The ath-
letes of the group without PMS showed no change in IL-6
concentration, leading us to believe that the IL-6 found
after the game in the PMS group had a proinflammatory
function, since the exercise did not appear to be intense
enough to increase the concentration of muscle-released
IL-6 in the group without PMS.
The increase in TNF-α observed in the group without
PMS after exercise in the follicular phase is compatible
with the inflammatory response normally observed after
vigorous exercise and is in agreement with the literature.
However, this result was not observed in the athletes with
PMS, suggesting that these athletes had an inflammatory
status that was not increased by the exercise as would
have been expected. An important aspect to consider is
the role of inflammation in behavioral changes, as it is
well established in the literature that mood states may be
influenced by proinflammatory cytokines such as IL-1β
and TNF-α [20].
The results of our study regarding mood states showed
differences between the group with PMS and the group
without PMS, with increased depression and tension only
in the group with PMS in the pre-game moments (fol-
licular and luteal phases, respectively), evidencing that
athletes with PMS may present major mood changes.
Gaion and Vieira [21] observed that PMS leads to nega-
tive changes in mood states of athletes during the pre-
menstrual period, especially on the last day before men-
struation.
The correlation results of our study evidenced a nega-
tive correlation between IL-10 and depression scores in
the follicular phase in the PMS group, which could be
interpreted as a possible mechanism of the organism try-
ing to control the exacerbation of the negative mood
state. A recent publication by our group (with the same
PMS, Inflammation, and Mood States in
Soccer Players
volunteers) [12] demonstrated that athletes with PMS
are more anxious than those without PMS. In addition,
we found a positive correlation between IL-10 and anxi-
ety levels in the PMS group, suggesting that subjects with
PMS produce more IL-10 in a failed attempt to control
anxiety.
The positive correlation found between IL-10 and
growth hormone strengthens the idea that athletes with
PMS try to maintain homeostasis and control the inflam-
matory process. A previous study by our group [22] on
marathon runners showed that the volunteers had elevat-
ed levels of IL-10, IL-8, and growth hormone before the
race, suggesting that these cytokines act as protective
mechanisms of the central nervous system when submit-
ted to strenuous exercise.
Conclusion
We were able to demonstrate that athletes with PMS
evidence an inflammatory state due to the syndrome, and
that this inflammation influences their behavior.
Acknowledgements
This project was developed with support from the São Paulo
Research Foundation (FAPESP; grant No. 2010/52424-0). This
work was also conducted during a scholarship supported by the
International Cooperation Program CAPES/COFECUB at the
Federal University of São Paulo and financed by CAPES – Brazil-
ian Federal Agency for Support and Evaluation of Graduate Edu-
cation within the Ministry of Education of Brazil. The funders had
no role in the study design, data collection and analysis, the deci-
sion to publish, or preparation of the manuscript.
Statement of Ethics
The study protocol and consent form were approved by the
Federal University of São Paulo Ethics Committee, Brazil (No.
1604/10).
Disclosure Statement
The authors have no conflicts of interest to disclose.
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Neuroimmunomodulation 5
DOI: 10.1159/000494559
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