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Probiotic supplementation in sports and physical exercise: Does it present any ergogenic effect?

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Background: Probiotics are live microorganisms that promote health benefits to the host. Evidence indicates that some probiotic strains play an immunomodulatory role and reduce the incidence of respiratory and gastrointestinal infections in athletes and in physical activity practitioners. For this reason, probiotic supplementation could indirectly improve exercise performance. However, recent studies have observed direct ergogenic effects of probiotics, but the mechanisms of action are poorly elucidated. Objective: In this study, we aim to synthesize available knowledge on the effect of probiotics on physical exercise, identify the mechanisms of action by which probiotics could improve performance directly and indirectly, and verify whether probiotics have any ergogenic effect. Methods: The study was performed in the PubMed database in February 2017, without limitation as to the publication period. The keyword combinations used were: 'Probiotics' and 'Sports' ( n = 17 articles), 'Probiotics' and 'Exercise' ( n = 26 articles) and 'Probiotics' and 'Athletes' ( n = 11 articles). Results: Of the 16 studies evaluated, only six applied performance tests, of which only two demonstrated that probiotic supplementation increases performance, but one of them was performed with mice. Conclusions: According to the studies evaluated, probiotic supplementation does not present ergogenic effect, however, considering the small number of studies, this subject should be better investigated.
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Article
Probiotic supplementation in sports
and physical exercise: Does it present
any ergogenic effect?
Audrey Yule Coqueiro
1
, Amanda Beatriz de Oliveira Garcia
1
,
Marcelo Macedo Rogero
2
and Julio Tirapegui
1
Abstract
Background: Probiotics are live microorganisms that promote health benefits to the host. Evidence indicates that some
probiotic strains play an immunomodulatory role and reduce the incidence of respiratory and gastrointestinal infections in
athletes and in physical activity practitioners. For this reason, probiotic supplementation could indirectly improve exercise
performance. However, recent studies have observed direct ergogenic effects of probiotics, but the mechanisms of action
are poorly elucidated. Objective: In this study, we aim to synthesize available knowledge on the effect of probiotics on
physical exercise, identify the mechanisms of action by which probiotics could improve performance directly and indir-
ectly, and verify whether probiotics have any ergogenic effect. Methods: The study was performed in the PubMed
database in February 2017, without limitation as to the publication period. The keyword combinations used were:
‘Probiotics’ and ‘Sports’ (n¼17 articles), ‘Probiotics’ and ‘Exercise’ (n¼26 articles) and ‘Probiotics’ and ‘Athletes’ (n¼11
articles). Results: Of the 16 studies evaluated, only six applied performance tests, of which only two demonstrated that
probiotic supplementation increases performance, but one of them was performed with mice. Conclusions: According
to the studies evaluated, probiotic supplementation does not present ergogenic effect, however, considering the small
number of studies, this subject should be better investigated.
Keywords
Probiotics, exercise, sports, athletes, performance-enhancing substances
Introduction
The practice of exhaustive physical exercises promotes
immunosuppression (Clancy et al., 2006) and oxidative
stress (Martarelli et al., 2011), states associated with the
increased incidence of upper respiratory tract infections
(URTIs) (Cox et al., 2010) and gastrointestinal tract (GIT)
disorders (Shing et al., 2014). These conditions usually
occur during competitive periods (more intense training
period), affecting the athlete’s health and impairing phys-
ical performance (West et al., 2011). In this context,
interventions that prevent or mitigate these conditions can
indirectly improve physical performance. Among the
nutritional supplements used in the modulation of the
immune response of athletes, probiotics can be highlighted
(Chen et al., 2016).
The concept of probiotics, according to the Food and
Agriculture Organization of the United States/World
Health Organization (FAO/WHO), refers to ‘live micro-
organisms that, when administered in adequate amounts,
confer a health benefit on the host’. Therefore, micro-
organisms that do not present health benefits or promote
adverse effects are not considered probiotics (FAO/WHO,
2002). The main health claims of probiotics are linked to
positive changes in microbiota composition, improving
intestinal health and homeostasis of the immune system,
which may act to reduce the risk and treat, as co-adjuvants,
gastrointestinal and immune diseases (Hill et al., 2014).
Recent studies indicate that probiotics can increase
exercise performance in physical activity practitioners and
athletes, not only indirectly, but also directly, by increasing
the availability of energy—the improvement in the intest-
inal microbiota composition is linked to an improvement in
1
Department of Food and Experimental Nutrition, Faculty of Pharma-
ceutical Sciences, University of Sa
˜o Paulo, Sa
˜o Paulo, Brazil
2
Department of Nutrition, Faculty of Public Health, University of Sa
˜o
Paulo, Sa
˜o Paulo, Brazil
Corresponding author:
Audrey Yule Coqueiro, Department of Food and Experimental Nutrition,
Faculty of Pharmaceutical Sciences, University of Sa
˜o Paulo, Avenida
Professor Lineu Prestes 580, Sa
˜o Paulo, CEP: 05508-000, Brazil.
Email: audreycoqueiro@hotmail.com
Nutrition and Health
2017, Vol. 23(4) 239–249
ªThe Author(s) 2017
Reprints and permission:
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DOI: 10.1177/0260106017721000
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the nutrient absorption process—by the synthesis of short-
chain fatty acids, which are used as energetic substrates, by
antioxidant action, which can attenuate muscle injury
induced by reactive oxygen species, among others (Chen
et al., 2016). However, the effect of probiotic supple-
mentation on physical exercise and sports is unclear,
especially regarding exercise performance.
In this sense, the aims of the present study were to
synthesize available knowledge on the effect of probiotics
on physical exercise and sports; to identify the mechanisms
by which probiotics could improve performance directly
and indirectly; and, finally, to verify whether probiotics
exert an ergogenic effect.
Material and methods
The study was carried out in the PubMed database in
February 2017, using the descriptor MeSH (Medical Sub-
ject Headings), without limitation as to the publication
period. The keyword combinations used were: ‘Probiotics’
and ‘Sports’ (n¼17 articles), ‘Probiotics’ and ‘Exercise’
(n¼26 articles) and ‘Probiotics’ and ‘Athletes’ (n¼11
articles).
Of the 54 articles, 19 were common to the three studies,
so the number of articles selected was 35. Of these, seven
articles had no correlation with the subject, and five articles
did not provide the complete version. Of the 23 remaining
articles, 14 are original (included in the article) and nine are
literature reviews, of which only two were included in the
article. In addition to these articles, two other original
studies, which were cited in the articles evaluated, but were
not obtained in the study, were included. Finally, we
included 16 original articles that evaluated the effect of
probiotic supplementation in sports and physical exercise.
In Figure 1, the above steps are presented.
Effects of probiotic supplementation on
immune system, upper respiratory tract
infections and gastrointestinal tract
disorders in active individuals and athletes
Exhaustive physical exercise negatively impacts on
immunocompetence, promoting a reduction of the count
and function of immune cells, such as natural killer (NK)
cells, neutrophils and T lymphocytes, increased plasma
concentration of pro-inflammatory biomarkers, and
reduced plasma concentration of anti-inflammatory cyto-
kines, among others (Clancy et al., 2006; Cox et al., 2010;
Lollo et al., 2012; Donmez et al., 2014). These facts are
associated with increased incidence of URTI and disorders
of the GIT (Clancy et al., 2006; Shing et al., 2014) that tend
to inhibit physical performance (West et al., 2011).
In order to attenuate or even reverse these deleterious
effects caused by exhaustive exercise, several nutritional
interventions have been used and probiotic supplementa-
tion is one of them. In this sense, Clancy et al. (2006)
evaluated the immunomodulatory effect of the probiotic
Lactobacillus acidophilus (2 10
10
colony-forming units
(CFU)/day), supplemented for 1 month to fatigued athletes
(fatigue was self-reported and athletes started the study
already fatigued), who presented characteristics of recur-
rent infection by the Epstein Barr virus (EBV), such as
Figure 1. Stages of study, selection and inclusion of articles.
240 Nutrition and Health 23(4)
reduction of interferon g(IFN g) secretion by TCD4
þ
(cluster of differentiation 4) cells. Probiotic treatment
increased the secretion of IFN gby T cells (ex vivo test) in
similar values to healthy individuals, but did not alter other
immunological parameters such as salivary IgA (immu-
noglobulin A) and IFN g. One of the limitations of this
study is the sample value, considering that the group of
fatigued athletes included only nine individuals. Another
limitation is that fatigue was self-reported, but not eval-
uated by biochemical and molecular parameters or physical
performance tests, among others.
Lollo et al. (2012) also found beneficial effects related
to the leukocyte count of rats after consumption of cheese
containing L. acidophilus LA14 and Bifidobacterium
longum BL05 (10
6
/10
7
CFU/day), for 14 days. Probiotic
supplementation increased the leukocyte and lymphocyte
counts that had been reduced after running on a treadmill
until exhaustion. In addition, the immature neutrophil count
was lower in the exercised and treated group compared
with the exercised group that had not received treatment.
Similarly, Donmez et al. (2014) observed that con-
sumption of homemade koumiss (mare’s milk fermented
with lactic acid bacteria, in special Lactobacillus del-
brueckii subspecies Bulgaricus,Lactobacillus salivarus,
Lactobacillus buchneri,Lactobacillus plantarum,Lacto-
bacillus casei,Lactobacillus helveticus,Lactobacillus fer-
mentum and yeasts, such as Saccharomyces lactis,Torula
koumiss,Kluyveromyces lactis and Saccharomyces uni-
sporus), 350 mL for 15 days, for individuals submitted to
aerobic exercise, promoted an increase in leukocyte and
neutrophil counts.
Unlike the studies mentioned above, Moreira et al.
(2007), in a randomized, double-blind, placebo-controlled
study, did not find positive results when supplementing
Lactobacillus GG (3 10
8
CFU/mL—130 mL per day)
for 3 months to marathon runners. This treatment did not
alter any of the immunological parameters analyzed,
such as eosinophil counts in the blood and total IgE
(immunoglobulin E) concentration, nor did it reduce the
incidence of asthma and allergies. The absence of an
immunomodulatory effect was also found in the study by
Gill et al. (2016) (blinded, randomized and counter-
balanced, crossover design), where the administration of
the probiotic L. casei (10
11
CFU/day) for 7 days to indi-
viduals submitted to running in hot environmental con-
ditions did not result in improvement in immunological
parameters related to the oral mucosa, such as salivary
IgA and salivary antimicrobial protein (S-AMP). How-
ever, this study consisted of only eight participants and the
duration of supplementation lasted just 7 days, limiting
the accuracy of the results.
In 2007, 47 male French officer cadets in commando
training were supplemented with L. casei strain DN-114
001 (the dose was not mentioned) for approximately
4 weeks in a randomized, double-blind, placebo-controlled
study. Only the placebo group had a reduction in salivary
IgA after training, indicating the immunomodulatory effect
of the probiotic. However, there was no statistically sig-
nificant difference between the groups in terms of URTI
incidence. It is worth noting that the probiotic dose was not
mentioned in the study, which makes the analysis of results
impossible, since the lack of effect could be due to insuf-
ficient dose (Tiollier et al., 2007).
In 2010, the immunomodulatory potential of another
bacterium of the Lactobacillus genus was investigated in
the sporting context, in a double-blind, placebo-controlled,
crossover trial. Cox et al. supplemented L. fermentum
VRI-003 (PCC) (1.2 10
10
CFU/day) for 1 month to elite
athletes during the winter (the period with the highest
incidence of respiratory infections) and observed that par-
ticipants reported fewer respiratory symptoms during sup-
plementation. The severity of respiratory diseases was also
lower during treatment. As in the study of Clancy et al.
(2006), there was no significant statistical difference in
other immunological parameters, such as salivary IgA and
IgA, IL-4 (interleukin 4) and IL-10 (interleukin 10) in the
serum, but there was an increase in the secretion of IFN gin
the treated group (ex vivo test with whole blood) compared
with placebo.
West et al. (2011) also evaluated the effect of the pro-
biotic L. fermentum (1 10
9
CFU/day) for 11 weeks, in a
double-blind, randomized, controlled trial. It was observed
that in competitive cyclists, the number and duration of
mild gastrointestinal symptoms (bloating, flatulence and
cramping) were twice as high in the probiotic group as
compared with the placebo group. The authors believe that
these symptoms are due to gastrointestinal adaptation to the
supplemented microorganism, which occurs in the first few
days of supplementation. However, supplementation was
offered for 11 weeks, and symptoms were described
throughout the experimental period. Respiratory symptoms
were lower in men supplemented with probiotics, but not in
treated women, in whom the number of respiratory symp-
toms increased. It is noteworthy that the same dose of
probiotic was offered to men and women, but the increase
of the microorganism in the faeces of men was higher
than that found in supplemented women; however, the
mechanism by which this occurred is poorly explained in
the study. In addition, immediately after training (any
physical exercise practiced by individuals), probiotic sup-
plementation attenuated the increase of pro- and anti-
inflammatory cytokines in the plasma (IL-1RA, IL-6,
IL-8, IL-10, GM-CSF, IFN g, TNF-a), however, this
result was not observed at rest, only immediately after
training. The authors emphasize that the reduction of
cytokine concentration in plasma, demonstrating the
absence of ‘disturbances’ in the immune system, could be
related to the reduction of susceptibility to infections.
Nonetheless, it is well established in the literature that the
reduction of anti-inflammatory cytokines, especially after
training, is not beneficial, considering the importance of
these cytokines in several processes, such as tissue repair
(Raizel et al., 2016). The reduction of cytokine concen-
tration occurred in supplemented men and women, but the
Coqueiro et al. 241
respiratory symptoms were only lower in men. This dis-
crepancy was not discussed in the study.
Haywood et al. (2014) continued to investigate the
effect of probiotic supplementation on the incidence,
severity and duration of URTI and GIT disorders, in a
randomized control trial with two arms; placebo and pro-
biotic. Rugby players were studied and were supplemented
with the probiotics Lactobacillus gasseri (2.6 10
9
CFU/
day), Bifidobacterium bifidum (2.0 10
8
CFU/day) and
B. longum (2.0 10
8
CFU/day) for 4 weeks and then with
placebo, also for 4 weeks, with a washout period of 4 weeks
between interventions. During probiotic treatment, 47%of
participants did not report any URTI or GIT disorder, while
in the placebo period, only 20%of participants reported no
symptoms. The infection duration was also lower with
probiotic supplementation, but there was no statistically
significant difference regarding disease severity.
In 2014, West et al., in a randomized double-blind
placebo-controlled trial, distributed 265 physically active
individuals into three groups: group 1: supplemented with
Bifidobacterium ani malis subsp.lactis Bl-04 (2.0 10
9
CFU/
day); group 2: supplemented with L. acidophilus NCFM
and B. animalis subsp. lactis Bi-07(5x10
9
CFU/day) and
group 3: placebo. The supplementation period was
164 days. The risk of developing URTI was lower group 1
compared with the placebo group, but there was no statis-
tically significant difference between group 2 and the
placebo group. The authors concluded that supplementa-
tion with B. animalis subsp. lactis Bl-04reducestheriskof
URTI; however, the study had some limitations, since
physical exercise was not controlled and group 2 was more
physically active compared with the placebo group.
In 2016, another two studies investigated probiotic
supplementation in the prevalence of URTI. Marinkovic
et al., in a randomized double-blind placebo-controlled
trial, supplemented elite athletes with L. helveticus (2
10
10
CFU/day) for 14 weeks during the winter period and
observed that the treatment reduced the duration of
respiratory infection, as well as the number of related
symptoms, but there was no difference between the
groups regarding the severity and duration of the illness.
The leukocyte count, and other parameters linked to the
immune system, such as serum TGF-b(transforming
growth factor beta), IL-10 and IFN gsecreted by per-
ipheral blood mononuclear cells (PBMCs) among others,
also did not differ with treatment.
Gleeson et al. (2016), in a randomized, double-blind,
placebo-controlled trial, evaluated the effect of the pro-
biotic L. casei Shirota (6.5 10
9
CFU twice a day) for 20
weeks in physically active individuals on the incidence,
severity and duration of URTI, EBV and cytomegalovirus
(CMV) serostatus, as well as on the concentration of anti-
bodies in the plasma. The incidence of URTI was low in
both groups, and there was no statistically significant dif-
ference between the probiotic and placebo groups. This
result may be because the sample consisted of physical
activity practitioners and non-athletes. Regular ingestion of
probiotics reduced the number of antibodies in EBV and
CMV. The authors interpreted this result as an immuno-
modulatory effect of the probiotic, since the level of CMV
is part of the immune-risk profile used to assess immune
dysregulation in elderly people. Similarly, changes in
plasma EBV could be used to evaluate any disorder in
overall immune status. Moreover, evidence indicates that
stress-related immunosuppression increases EBV and
CMV antibody titers.
Beside the negative impact related to immunocompe-
tence, the practice of exhausting physical exercises is
associated with the development of oxidative stress. In this
context, Martarelli et al., in 2011, evaluated the effect of
the microorganisms Lactobacillus rhamnosus IMC 501
and Lactobacillus paracasei IMC 502
(10
9
CFU/day of a
mixture of the two probiotics) for 4 weeks on oxidative
stress parameters (measured by performing the dROMs
test, which determines the level of reactive oxygen meta-
bolites) in athletes. As expected, intense physical exercise
induced oxidative stress, but probiotic supplementation
increased the concentration of plasma antioxidants (per-
formed by the biological antioxidant potential (BAP) test,
which measures plasma levels of antioxidants), attenuating
the deleterious action of reactive oxygen species.
According to the authors, the mechanisms by which
probiotics present antioxidant effects are linked to the
synthesis of antioxidant substances such as vitamins B1, B5
and B6, by microorganisms. Moreover, probiotic supple-
mentation reduces the risk of conditions linked to oxidative
stress, such as hyperglycemia. Finally, the improvement in
intestinal homeostasis, including the absorption process,
may favor the absorption of antioxidants, increasing the
availability of these substances (Martarelli et al., 2011).
Although this study did not evaluate individual perfor-
mance, it can be verified that oxidative stress promotes
muscle injury, which is linked to the development of fati-
gue (Finsterer, 2012). In this context, the attenuation of
oxidative stress and, consequently, muscle injury, could
promote fatigue delay and improve physical performance.
Valimaki et al. (2012) also aimed to evaluate the
antioxidant effect of probiotics, in a randomized, double-
blind, placebo-controlled parallel-group intervention study.
However, unlike the study by Martarelli et al. (2011), they
did not observe any effect of probiotic supplementation on
oxidative stress. Marathon runners that were supple-
mented with L. rhamnosus GG (3.0 10
8
CFU/mL—
65 mL per day) for 3 months did not present changes in
the parameters of oxidative stress evaluated: oxidized
low-density lipoprotein, antioxidant potential s-total
radical-trapping antioxidant assay and serum antioxidants
(s-a-tocopherol, s-g-tocopherol, s-retinol, s-b-carotene,
and s-ubiquinone-10).
Although most of these studies have shown positive
effects of probiotics on the health of physical activity
practitioners and athletes, most of them do not evaluate
exercise performance. Therefore, it is not possible to
evaluate whether the immunomodulatory and antioxidant
242 Nutrition and Health 23(4)
effect induced by the ingestion of the probiotic influenced
the physical performance.
The abovementioned studies are presented in table 1.
Effects of probiotic supplementation on sports
performance and proposed mechanisms of action
The main aim of most of the studies reported was to
evaluate the effect of probiotics on immunocompetence,
that is, the reduction of the incidence, duration and severity
of infections and immunocompetence definition. However,
in some of the aforementioned studies, the athletic per-
formance of the individuals was evaluated.
Cox et al. (2010) applied performance treadmill running
tests at the beginning and end of the experiment. These
tests consisted of a continuous incremental running of
3/4-minute periods at 14, 16 and 18 km/h at 0%gradient.
After 2 minutes of rest, the individuals started running
again at a speed of 18 km/h, that was increased by 1 km/h
each minute for 3 minutes at 0%gradient. The speed was
maintained at 20 km/h and the gradient increased by 1%per
minute for a minute until volitional exhaustion. There was
no statistically significant difference in the supplemented
(L. fermentum VRI-003, 1.2 10
10
CFU/day, for 1 month)
or placebo period, indicating that probiotic supplementa-
tion did not affect physical performance in elite athletes.
Similarly, in the study of West et al. (2011), there was
no difference between groups in incremental perfor-
mance tests on a cycle ergometer, maximal oxygen
uptake (VO
2max
) and exercise session duration, indicat-
ing that probiotic supplementation (L. fermentum,110
9
CFU/
day for 11 weeks) did not improve physical performance
in competitive cyclists.
In 2016, two other studies did not observe an ergogenic
effect after probiotic supplementation. Gill et al. observed
that probiotic supplementation (L. casei,10
11
CFU/day for
7 days) did not influence the exercise performance on a
treadmill test, for 2 hours, at 60%of VO
2max
, and the
perception of effort in individuals submitted to running in
hot environmental conditions. In addition, Marinkovic
et al. (2016) verified that the supplementation of L. hel-
veticus (2 10
10
CFU/day for 14 weeks) for elite athletes
did not improve exercise performance (VO
2max
, exercise
duration and maximal heart rate), but the self-reported
vigor of the participants was higher in the group treated
with probiotics. However, this result was evaluated by a
questionnaire, being subjective and representing a limita-
tion of the study.
On the other hand, certain studies indicate an ergogenic
effect of probiotic supplementation. Shing et al. (2014), in a
double-blind, placebo-controlled, crossover trial supple-
mented runners with a mix of probiotics containing nine
strains (L. acidophilus—7.4 10
9
CFU/day, L. rhamno-
sus—15.55 10
9
CFU/day, L. casei—9.45 10
9
CFU/
day, L. plantarum—3.15 10
9
CFU/day, L. fermentum
1.35 10
9
CFU/day, Bifidobacterium lactis—4.05 x 10
9
CFU/day, Bifidobacterium breve—1.35 10
9
CFU/day,
B. bifidum—0.45 10
9
CFU/day and Streptococcus ther-
mophilus—2.25 10
9
CFU/day) for 4 weeks. After treat-
ment, the runners were submitted to a fatigue test on a
treadmill at 80%of their ventilatory threshold, in hot
environmental conditions (35 C and 40%humidity). To
determine the ventilatory threshold for each runner, a
VO
2max
test was performed. The test started at 10 km/h,
0%gradient,withthespeedincreasingby1km/hper
minute until a speed of 18 km/h. After one minute at
18 km/h, the treadmill gradient was increased by 1%each
minute until fatigue.
It was observed that probiotic supplementation pro-
moted an increase in the time until fatigue, however the
authors emphasize that they do not know the mechanisms
by which this result occurred, since probiotic supple-
mentation did not improve the intestinal permeability and
had little influence on inflammatory parameters (IL-1ra,
IL-6 and IL-10 in the plasma), except for serum lipopoly-
saccharide. This parameter was higher in placebo (at rest
and after training) compared with the probiotic period,
indicating that probiotic supplementation reduced systemic
inflammatory response. This study suggests that probiotics
have a direct effect on physical performance, but the
mechanisms of action are poorly known and therefore
should be investigated. It is worth noting that this study
administered different types of microorganisms, making it
difficult to identify which of them present an ergogenic
effect or even whether the effect is due to the synergism
between two or more microorganisms. Another issue is that
the dose administered was higher compared with the other
studies. Thus, the ergogenic effect may be dose-dependent.
In 2016, Chen et al. supplemented mice with L. plantarum
in different doses (2.05 10
8
or 1.03 10
9
CFU/kg/day)
for 6 weeks and observed that the treated animals, with both
doses offered, showed an increase in their relative mus-
cular weight. However, all other results were dose-
dependent and only occurred with the highest dose.
Supplementation increased muscle strength (measured by
grip strength) and duration of swimming performance test,
with load corresponding to 5%of mice body weight, (the
supplemented group with the lowest dose having a duration
88%higher than the placebo group—9.0 +0.6 minutes,
while the group supplemented with the highest dose had a
duration 383%higher than the placebo group—23.2 +1.4
minutes. The mean of the placebo group duration was
4.8 +0.9 minutes). Probiotic supplementation also increased
the number of type I muscle fibers in the gastrocnemius
muscle, however, authors did not mention how this result
occurred (mechanism of action), making data interpretation
difficult. Moreover, probiotic supplementation increased
muscle strength but did not affect type II muscle fibers.
Authors also did not discuss this result.
Treated animals also showed a reduction in the con-
centration of lactate, ammonia, creatine kinase (CK) and
serum glucose in the post-training period. Beside the
effects of physical activity, treated animals also presented a
reduction in serum albumin, serum urea and creatinine, as
Coqueiro et al. 243
Table 1. Effects of probiotic supplementation on physical exercise.
nAge Exercise modality Probiotic and dose Treatment duration Probiotic effects Reference
27 individuals (18 healthy
athletes and 9 fatigued
athletes—17 males and
10 females)
16–40 y Fatigued athletes Lactobacillus acidophilus
210
10
CFU/day
1 month Increase in IFN gsecretion by T cells Clancy et al., 2006
141 non-elite marathon
runners (123 males and
16 females)
30–40 y Running marathon Lactobacillus GG
310
8
CFU/mL Participants
drank 130 mL/day
3 months No effect Moreira et al., 2007
47 male cadets 20–22 y Military training Lactobacillus casei strain DN-114 001
The dose was not mentioned
3 weeks of military
training þ5 days
of combat
Probiotics supplementation
prevented the reduction of salivary
IgA after training There was no
difference between groups on
URTI incidence
Tiollier et al., 2007
20 elite male distance
runners
20–34 y Running (competing in events
ranging from 800 m to the
marathon, 42.2 km)
Lactobacillus fermentum VRI-003
(PCC)
1.2 10
10
CFU/day
1 month Reduction in respiratory symptoms
and in the severity of respiratory
infections Increase in IFN g
secretion
Cox et al., 2010
99 competitive cyclists (64
males and 35 females)
26–44 y Cycling Lactobacillus fermentum (PCC
)
10
9
CFU/day
11 weeks Probiotics supplementation increased
the number and duration of mild
gastrointestinal symptoms, but
improved respiratory symptoms in
men, but not women; in fact, there
was an increase in respiratory
symptoms in women supplemented
with probiotic Immediately after
training, there was a reduction in
plasma cytokines in the probiotics
group
West et al., 2011
24 males 25–39 y Running Lactobacillus rhamnosus IMC 501
and Lactobacillus
paracasei IMC 502
—10
9
CFU/day of a mixture of the two
probiotics
4 weeks Increase in plasma antioxidant levels Martarelli et al., 2011
119 marathon runners
(105 males 14 females)
22–58 y Running marathon Lactobacillus rhamnosus GG
3.0 10
8
CFU/mL Individuals
drank 65 mL per day
3 months No effect Valimaki et al., 2012
Male Wistar rats (there is
no mention of the total
n)
21-daysold Running on treadmill until
exhaustion
Cheese containing Lactobacillus
acidophilus LA14 and
Bifidobacterium longum BL05
10
6
/10
7
CFU/day
14 days Increase in the lymphocyte count Lollo et al., 2012
(continued)
244
Table 1. (continued)
nAge Exercise modality Probiotic and dose Treatment duration Probiotic effects Reference
30 male elite rugby union
players
20–28 y Rugby, gym work, weights, skills
and fitness tests
Lactobacillus gasseri (2.6 10
9
CFU/
day), Bifidobacterium bifidum (2.0
10
8
CFU/day) Bifidobacterium
longum (2.0 10
8
CFU/day)
4 weeks Reduction in respiratory and
gastrointestinal symptoms, and in
infection duration
Haywood et al., 2014
465 individuals (241 males
and 224 females)
23–48 y Gym work Bifidobacterium animalis subsp. lactis
Bl-04—2.0 10
9
CFU/day (group
1);
Lactobacillus acidophilus NCFM and
Bifidobacterium animalis subsp.
lactis Bi-07 (NCFM and Bi-07) 5
10
9
CFU/day (group 2)
164 days B1-04 reduced the risk of URTI West et al., 2014
18 males 30–37 y Aerobic exercise—60 minutes
per day and five times per
week
350 mL koumiss a day, fermented
with lactobacilli and yeasts
15 days Increase in the count of leukocytes
and neutrophils
Donmez et al., 2014
8 males 20–32 y Running exercise in hot ambient
conditions
Lactobacillus casei 10
11
CFU/day 7 days No effect Gill et al., 2016
39 elite athletes 18–28 y Athletes who trained more than
11 h/week Modalities:
badminton, triathlon, cycling,
alpinism,
athletics, karate, savate, kayak,
judo, tennis or swimming
Lactobacillus helveticus Lafti
L10 2
10
10
CFU/day
14 weeks Reduction of respiratory infection
duration and symptoms, but not
the incidence and severity
Marinkovic et al.,
2016
243 physically active
individuals (126
probiotics and 117
placebo—142 males and
101 females)
18–32 y Endurance sports (swimming,
cycling etc), individual sports
(tennis, squash etc) and team
games (rugby, football etc).
Lactobacillus casei Shirota
6.5 10
9
CFU in each pot
Individuals ingested the
supplement twice a day
20 weeks Probiotic supplementation reduced
plasma EBV and CMV antibody
titres.
Gleeson et al., 2016
CFU: colony-forming units; IFN: interferon; EBV: Epstein Barr virus; CMV: cytomegalovirus.
245
well as a reduction in triacylglycerol concentrations. The
authors conclude that supplementation with the probiotic
L. plantarum increases muscle mass, improves exercise
performance and has an anti-fatigue effect.
However, they affirm that lactate synthesis is linked
to the acidification of the intracellular environment,
and therefore the reduction of plasma lactate has been
considered beneficial. Meanwhile, this lactate concept was
overcome, since the synthesis of lactate through various
mechanisms attenuates acidosis, contrary to what was
believed (revised in Adeva-Andany et al., 2014). There-
fore, lactate concentration has recently been evaluated as
an intensity parameter in strength exercises. In this sense,
the lactate results shown by Chen et al. (2016) should be
evaluated with care. Nonetheless, other important fatigue
markers were reduced with probiotic supplementation,
such as ammonia, urea, CK and creatinine in the serum,
emphasizing that this microorganism supplementation has
potential to delay the development of fatigue.
The authors propose that probiotics could delay fatigue
by increasing energy availability through the synthesis of
short chain fatty acids. In addition, bacteria of the Lacto-
bacillus genus synthesize lactic acid, which is converted to
butyrate and later to acetyl-CoA, which is used in the
Krebs Cycle to generate adenosine triphosphate (ATP).
Notwithstanding, both processes occur mostly in the gut;
not in skeletal muscle to directly delay fatigue.
The aforementioned studies are presented in table 2.
Discussion and conclusions: after all, what
are the effects of probiotics on physical
exercise? Do they have an ergogenic effect
or not?
Most of the studies examined supplements with bacteria of
the Lactobacillus and Bifidobacterium genera. Of the 16
articles evaluated, 12 presented some beneficial effect from
probiotic supplementation; 3 did not present any type of
effect (beneficial or deleterious) and 1 presented adverse
effects, considering that supplementation promoted an
increase in mild gastrointestinal symptoms.
The main beneficial effects are linked to the immune
system:
1. Increased secretion of IFN gby immune cells;
2. Preventing the reduction of salivary IgA concentra-
tions in post-training. These data are conflicting,
considering that other studies have evaluated IgA
in saliva and serum and found no alterations from
probiotic supplementation;
3. Increased immune cell counts and function;
4. Reduction in incidence, duration and severity of
URTI. This result is also conflicting, since one
study presented this effect only in men and others
did not observe any type of alteration from
supplementation;
5. Antioxidant activity. Other articles have failed to
demonstrate any kind of antioxidant effect of
probiotics, so these data are also considered
conflicting.
It is worth mentioning that in one of the studies, there
was an increase in gastrointestinal symptoms, so the use
of probiotics should be carried out with caution. In clin-
ical practice, it is common sense that probiotic supple-
mentation should be implemented for at least 14 days
prior to competition or important events for the athlete,
given that during this period the gastrointestinal tract
adapts to the administered microorganism, and there
may be mild gastrointestinal symptoms, such as flatu-
lence (Pyne et al., 2015).
Only six studies have evaluated the performance, just
two of which observed improvement in exercise perfor-
mance, but one was performed with mice. Both studies
administered L. plantarum, isolated (Chen et al., 2016), or
in a mix of probiotics (Shing et al., 2014). Therefore, it
could be speculated that this probiotic (L. plantarum) has
an ergogenic effect. The development of studies adminis-
tering L. plantarum to physical activity practitioners and
athletes is important in attempting to elucidate this issue.
Nevertheless, most evidence indicates that probiotic sup-
plementation has no ergogenic effect.
Finally, certain considerations will be made regarding
possible methodological failures of the studies. Evidence
indicates discrepancies between men and women, even
after supplementation of probiotics with the same dose. In
this sense, in studies with both sexes, conflicting results
may follow from this fact. However, the recommendation
was no different for men and women, necessitating studies
about this topic, with the intention of establishing a rec-
ommendation for each sex.
1. The small number of volunteers may also compro-
mise accuracy of results.
2. The short period of supplementation is also an
important factor. As previously mentioned, the time
of adaptation of the organism to the probiotic is
approximately 14 days. Thus, studies that supple-
ment for a similar or shorter period should be eval-
uated with caution. Evidence indicates that, with the
interruption of probiotic intake, there is a reduction
in the microorganism administered in the colon, and
with 8 days of supplementation discontinuation, the
probiotic is no longer detectable in the gut (Kullen
et al., 1997).
3. Since many effects are dose-dependent, the dose
administered is an important factor to be consid-
ered. The probiotic recommendation is, approxi-
mately, 10
8
–10
9
CFU/day, however, this value
varies in each country (Anvisa, 2008; Ministerio
Della Salute, 2013). There is no specific probiotic
recommendation for athletes or physical activity
practitioners.
246 Nutrition and Health 23(4)
Table 2. Effects of probiotic supplementation on exercise performance.
nAge Exercise modality Probiotic and dose
Treatment
duration Probiotic effects Reference
20 elite male
distance
runners
20–34 y Running (competing in events
ranging from 800 m to the
marathon 42.2 km)
Lactobacillus fermentum VRI-003 (PCC)
1.2 10
10
CFU/day
1 month There was no difference between groups on
treadmill running tests until exhaustion
Cox et al., 2010
99 competitive
cyclists (64
males and 35
females)
26–44 y Cycling Lactobacillus fermentum (PCC
)10
9
CFU/day 11 weeks There was no difference between groups in
the incremental performance tests on a
cycle ergometer, VO
2max
and exercise
session duration
West et al., 2011
10 male runners 25–29 y Running in heat conditions 7.4 10
9
CFU/day of L. acidophilus, 15.55
10
9
CFU/day of L. rhamnosus, 9.45 10
9
CFU/day of L. casei, 3.15 10
9
CFU/day of L.
plantarum, 1.35 10
9
CFU/day of L.
fermentum, 4.05 10
9
CFU/day of B. lactis,
1.35 10
9
CFU/day of B. breve, 0.45 10
9
CFU/day of B. bifidum and 2.25 10
9
CFU/
day of S. thermophilus
4 weeks Increase in the time until fatigue in a test on a
treadmill, at 80% of ventilatory threshold, in
hot environmental conditions
Shing et al., 2014
8 males 20–32 y Running exercise in hot ambient
conditions
Lactobacillus casei 10
11
CFU/day 7 days There was no difference in exercise
performance on a treadmill test and the
perception of effort
Gill et al., 2016
39 elite athletes 18–28 y Athletes who trained more than
11 h/week Modalities:
badminton, triathlon, cycling,
alpinism,
athletics, karate, savate, kayak,
Judo, tennis or swimming
Lactobacillus helveticus Lafti
L10 2 10
10
CFU/day
14 weeks There was no difference in exercise
performance, VO
2max
, exercise duration
and maximum heart rate between groups,
but probiotic supplementation increased
the sense of vigor
Marinkovic et al.,
2016
24 male mice Not mentioned Swimming Lactobacillus plantarum TWK10 (LP10)
2.05 10
8
or 1.03 10
9
CFU/kg/day
6 weeks Increase in exercise performance in swimming
test, with 5% of body weight
Beside that, probiotic supplementation
increased muscle mass and type I muscle
fibers, reduced serum lactate, ammonia, CK,
glucose, albumin, urea, creatinine and
triacylglycerol
Chen et al., 2016
CFU: colony-forming units; VO
2max
: maximal oxygen uptake, CK: creatine kinase.
247
4. Most of the studies did not control the individuals’
level of physical activity, so individuals in the same
study may have very different levels of physical
activity, making comparison impossible.
5. No studies were found that evaluated the perfor-
mance in strength exercises after supplementation
with probiotics and this can be seen as an important
niche to be studied.
Author contributions
Initial manuscript preparation was performed by AYC and
ABOG, and revised by MMR. The final manuscript version
was revised by JT.
Declaration of conflicting interests
The authors declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of
this article.
Funding
The authors disclosed receipt of the following financial
support for the research, authorship, and/or publication of
this article: The authors would like to thank the Sa
˜o Paulo
Research Foundation (FAPESP, number 2016/04910-0)
and the Brazilian National Council for Scientific and Tech-
nological Development (CNPq) for the grants.
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