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Artigo Sobre Nutrição, Exercício e Microbiota Intestinal
Artigo Sobre Nutrição, Exercício e Microbiota Intestinal
UMR PNCA, Agro Paris Tech, INRA, University Paris-Saclay, Paris, France
2
*Corresponding authors: AH Lancha Jr, School of Physical Education and Sport, University of São Paulo, Brazil, Tel:
+33144088676, E-mail: lanchajr@usp.br;
F Blachier, UMR PNCA, Agro Paris Tech, INRA, University Paris-Saclay, Paris, France, Tel: +33144088675, Fax: +33144081858,
E-mail: francois.blachier@agroparistech.fr
Citation: Costa AV, Leite G, Resende A, Blachier F, AH Lancha Jr (2017) Exercise, Nutrition and Gut
Microbiota: Possible Links and Consequences. Int J Sports Exerc Med 3:069. doi.org/10.23937/2469-
5718/1510069
Received: July 13, 2016; Accepted: August 21, 2017; Published: August 24, 2017
Copyright: © 2017 Costa AV, et al. This is an open-access article distributed under the terms of the
Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction
in any medium, provided the original author and source are credited.
Liu, et al. [31] Voluntary Animals Model of LCR V4 region 16S rRNA, Exercise decreased the abundance
exercise; 11 (Ovariectomized and HCR in Illumina MiSeq of Firmicutes in LCR and increased
weeks female rats) exercise and in HCR group. Also, it was capable
sedentary to increase Proteobacteria and
groups; all Cyanobacteria phyla in LCR, but
groups with decreased in HCR group. At family
HFD level, exercise decreased the
abundance of Ruminococcaceae
and Lachnospiraceae in LCR,
but increased in HCR. Exercise
increased Clostridiaceae and,
mainly, Clostridium genus, in both
exercise groups.
Mika, et al. [34] Voluntary Animals Healthy V4 region 16S rRNA, The juvenile runners, although
exercise; 6 juveniles and qPCR less diverse and richness than
weeks adults with their adults counterparts, showed
exercise and more changes as an increase in
sedentary Bacteroidetes and a decrease in
groups Firmicutes and Proteobacteria
phyla, which remains over 25 days
even without exercise.
Campbell, et al. Voluntary Animals Model of ND TRFLP and 454 GS Allobaculum spp. and Clostridiales
[26] exercise; 12 and HFD in FLX 454 Genome were enriched within the exercise
weeks exercise and Sequencer platform group in ND. Faecalibacterium
sedentary (pyrosequencing) prausnitzi was detected only in
groups exercise groups in both ND and
HFD and Lachnospiraceae was
not present in the HFD-e or HFD-s
groups.
Denou, et al. Controlled Animals Model of ND V3 region 16S rRNA, HIIT increased the overall
[33] exercise; HIIT; and obesity- Illumina MiSeq and richness of the microbiota in the
3 d/week; 6 inducing HFD qPCR colon of obese mice, mainly,
weeks in exercise within Bacteroidetes phylum and
and sedentary Bacteroidales order unlike to the gut
groups microbiota composition in HFD-s
group.
Clarke, et al. No intervention Humans Athletes V4 region 16S Athletes showed a higher
[27] (rugby players) rRNA, 454 Genome richness with less abundance of
and healthy Sequencer Bacteroidetes phylum. The family
untrained FLX platform Akkermansiaceae and the genus
controls (pyrosequencing) Akkermansia showed higher
levels in athletes when compared
to control group with high BMI
and lower levels of Bacteroides,
Lactobacillaceae and Lactobacillus
when compared to control group
with low BMI.
d: day; LIT: Low Intensity Training; HIIT: High Intensity Interval Training; LFD: Low Fat Diet; ND: Normal Diet; HFD: High Fat Diet;
LFD-e: Low Fat Diet plus exercise; LFD-s: Low Fat Diet within sedentary group; HFD-e: High Fat Diet plus exercise; HFD-s: High
Fat Diet within sedentary group; LCR: Low Capacity Running; HCR: High Capacity Running.
modifies the bacterial balance in the gut, with alteration only in the group submitted to exercise, as we observe
of the major phyla levels, and increase of the relative on Evans, et al. [25] research, hence supporting the hy-
proportion of butyrate-producing bacteria (Clostridia- pothesis that exercise causes changes in gut microbiota
ceae, Lachnospiraceae and Ruminococcaceae). The au- independent of changes in diet [26].
thors appoint that the exercise practice would be able
Short term (6 days) voluntary exercise showed that
to prevent the effects of a High Fat Diet (HFD) [25]. In
nutritional status and physical activity alter gut micro-
fact, Campbell, et al. [26] showed that exercise is able
biota diversity in different manners. When exercise is
to modify not only the specific populations of commen-
sal bacteria in the gut, but also cause morphological combinated with food restriction protocol (restricting
changes in gut microenvironment. In the Campbell et al. access for 23 hours per day and confined to running
study [26], the exercised group showed reduced intes- wheels except during a 60 min meal), a negative impact
tinal inflammation due to a high-fat diet and morpho- on bacterial richness is reported with respect to the Lac-
logical characteristics similar to the control. Likewise, in tobacillus and Bifidobacterium genera [30]. The caloric
a previous study, Faecalibacterium prausnitzi and Lach- restriction was also able to modify the phyla, even in
nospiraceae group (a Clostridia-cluster) were detected the presence of exercise [30] (Table 1). It seems that ex-
ercise cannot attenuate the effect of caloric restriction, more plastic and sensitive to environmental changes
whereas it would be able to cause improvements on gut during early life. Then, exercise initiated during the ju-
microbiota composition even under high fat diets. venile period may show a more robust impact on the
Voluntary exercise with different aerobic capacities, gut microbiota than exercise initiated in adulthood [34].
intensity, volume and frequency may present differ- In other words, the changes that occur in childhood may
ent outcomes. Evans, et al. [25] showed a significant last longer even with the absence of exercise than the
increase in the abundance of Bacteroidetes, while the changes occurring later. The authors show that exer-
evidence provided by Liu, et al. [31] showed a reduc- cise-induced alterations in microbiota during early life
tion in the abundance of Firmicutes and Proteobacteria contribute to metabolic consequences such as increased
phylum. Apart from both studies exposing the animals SCFA production, increased energy expenditure and re-
to the same diet (HFD), these differences observed be- duced fat accumulation in the adipose tissue. Indeed,
tween these two studies may originate from the differ- increased Bacteroidetes phyla along with decreased Fir-
ent experimental models used. Liu, et al. [31] study was micutes phyla within the gut have been associated with
performed with ovariectomized female rats fed with these metabolic consequences. The results obtained by
HFD, divided in High Capacity Running (HCR) and Low Denou, et al. [33] reinforce this proposition [33-35].
Capacity Running (LCR), performed 11 weeks of volun- It is important to observe that only one study regard-
tary exercise whereas Evans, et al. [25] performed 12 ing gut microbiota and exercise science was carried out
weeks voluntary exercise in male rats [25,31].
with athletes [27], a population in which the amount of
Petriz, et al. [32] proposed that training status and exercise training is very large and intense, and its out-
intensity may be favorable to the proliferation of spe- comes are different when compared with voluntary ex-
cific families of bacteria [32]. The authors reported an ercise performed in some animals’ protocols or short
inverse correlation between exercise and Clostridiace- session of moderate exercise performed by active indi-
ae/Bacteroideae families and Ruminococus genera, and viduals, as shown in Table 1.
a positive correlation between Oscillospira in exercise
intensity. Aerobic training may be associated with a Possible Mechanisms Connecting Physical Ex-
favorable environment for Clostridiaceae, Bacteroide- ercise and Gut Microbiota
ae and Ruminococus, but an unfavorable environment The effect of exercise on microbiota is still largely un-
for Oscillospira due to acidification of the intestinal known. They are likely to be mediated, at least in part,
environment. The proposition by Petriz, et al. [32] is in by altering parameters that influence the intestinal mi-
agreement with modification of the gut environment croenvironment.
following high intensity or long period exercise. Exer-
cise should modify the environment in a favorable way Short chain fat acids
in terms of anaerobic bacteria population, or acidic en- Exercise may increase butyrate-producing bacteria
vironment since a decrease splanchnic blood flow and species [25,28]. Matsumoto, et al. [28] were the first to
oxygen supply occurs [32]. show that chronic voluntary physical exercise in animals
A recent study performed using High Intensity In- is able to change SCFA production (n-butyrate) in the ce-
terval Training (HIIT), demonstrated that HIIT exerts cum with modifications in butyrate-producing bacteria
opposed changes to the gut microbiota compared to species. In addition, this study reported alteration in the
those imposed by obesity profile. Indeed, HIIT reduces cecal microbiota profile after exercise. These authors
the predicted metabolic genetic capacity of the fecal explain that part of the beneficial effects of exercise re-
microbiota, alters microbiota metabolic pathways, and lated to microbiota and subsequent variations in intesti-
raises the possibility that this type of exercise training nal health may be related to changes in the SCFA profile,
may elicit some of its beneficial effects on metabolism especially for butyrate concentrations [28]. This shift in
through alterations in the gut microbiome [33]. Howev- butyrate bacteria production in exercise group was also
er, this same study did not compare the different types shown by Evans, et al. [25].
of exercise, such as continuous versus intermittent, or
voluntary versus controlled exercise. These parameters The influence of physical exercise on the composi-
should be taken into consideration in future investiga- tion of the microbial environment has been linked to a
tions, since it remains unclear if the different types of decreased pH in the gut from SCFA production. Specifi-
exercise can cause similar beneficial effects regarding cally butyrate promotes cell differentiation and cell cy-
gut microbiota, and intestinal health as suggested by cle arrest, inhibits the enzyme histone deacetylase, and
Liu, et al. and Petriz, et al. [31,32]. decreases the transformation of primary to secondary
bile acids promoting colonic acidification [36]. Changes
Related to the beneficial impact of exercise on the in intestinal luminal pH may modify the environment in
microbiota composition and diversity in the early life, such way that it becomes more favorable for the prolif-
Mika, et al. [34] propose, “The sooner, the better”. This eration of some bacterial species [37].
proposition is related with the fact that microbiota is
Studies also have shown that butyrate may induce stantial changes in the cecal microbiome composition
mucin synthesis [38], and improve gut integrity by in- by stimulating the growth of Firmicutes at the expense
creasing tight junction assembly [34,39,40]. Mucins are of Bacteroidetes; and provoked outgrowth of several
the protective layer consisting of glycoproteins that help bacteria in the Clostridia and Erysipelotrichi classes [44].
forming the mucosal barrier lining of gastrointestinal Antimicrobial activity of the bile acids may elicit selec-
tract. This mucin layer has been recognized to play an tive pressure on the bacterial communities in exercised
important role for the interaction with gut microbiota, mice, leading to a shift of the gut microbiota composi-
and may serve as a substrate for intestinal bacteria, as tion [11].
Akkermansia muciniphila, and may alter the microbial
community composition [41].
Conclusion and Perspectives
Exercise and diet are considered as possible factors
Butyrate production in the large intestine is associ-
ated with production of Heat shock protein 70 (Hsp70). capable of modulating the intestinal balance between
Hsp70 maintains the functional and structural proper- the hosts by independent manners. Exercise has been
ties of intestinal epithelial cells in response to intense shown to improve the diversity of bacterial species and
exercise [42]. Since physical exercise and butyrate stim- richness under different nutritional strategies thus al-
ulate epithelial cell Hsp70 production, this may provide lowing for instance to reduce the negative effects of
structural and functional stability to intestinal epithelial high fat diet. The modification in short chain fatty acids
cells undergoing unfavorable conditions [25] ( Figure 1). production and alteration in intestinal pH appear to be
the main forms by which exercise may affect gut micro-
Bile acids biota composition.
Physical activity has been reported to increase excre- It is important to note that, the studies performed up
tion of primary bile acids in the gastrointestinal tract. to now, used solely the voluntary exercise as model. The
Since butyrate (that has been reported to be increased influence of specific features related to exercise train-
by physical activity) diminishes the conversion of bile ac- ing, such as volume, intensity, types of exercise (aerobic
ids into secondary bile acids, physical activity may con- or anaerobic or combination) may impact gut microbio-
sequently favor the rising of primary bile acids concen- ta in different ways. Likewise, changes in the diet and/
trations in the intestinal luminal content [23]. or different pathological conditions in the experimen-
The primary bile acids have established anti-micro- tal design raise some difficulties in evaluating only the
bial activity. In agreement with this hypothesis, Islam, exercise effect on the gut microbiota composition and
et al. [43] demonstrated that cholic acid induced sub- metabolic activity, as well as in comparing the results
Figure 1: Schematic view representing the possible ways by which physical exercise may impact the gut microbiota. This
includes Short-Chain Fatty Acid (SCFA) production by the microbiota, and bile acid production, as well as related alteration
of the luminal pH. Exercise may also impact gut transit time and intestinal immune response, which in turn may modify the
microbiota composition and metabolic activity.
obtained in different studies and this may hinder our The universality of maternal microbial transmission. PLoS
understanding. Biol 11: e1001631.
14. Cerdá B, Pérez M, Pérez-santiago JD, Tornero-aguilera JF,
Further experiments, including molecular biology González-soltero R, et al. (2016) Gut microbiota modifica-
studies, are obviously required in order to delineate the tion : another piece in the puzzle of the benefits of physical
precise mechanisms by which exercise impacts the in- exercise in health? Front Physiol 7: 51.
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This represents an important research area given the
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