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Prevention of acute GI disturbances with a functional food
formulation designed to support and maintain intestinal
barrier function during sports performance
Nicola Sponsiello1, Stefano Belgeri2, Roberto Conte2, Daniele Carandini2, Maurizio Salamone2
1Italian Society of Sport Nutrition and Wellness (SINSeB); 2Metagenics, Italy.
Summary. Gastrointestinal disturbances are very frequent among athletes undergoing strenuous and continuous
training and an endurance race. We tested a mix of nutrients and antioxidants for preventing GI disturbances and
dropouts at the “Tor des Geantes” ultratrail competition (330 km run). Athlets used the mix during training and
competition and showed benefits, including more power and resistance and better gastrointestinal health. Even if
not all of athletes took the mix on a regular basis during the race, the number of athletes pulling out of the race
due to gastrointestinal problems was 4.2% (1/24) in the treatment group compared to 11.3% (6/52) in the control
group.
Key words: gastrointestinal disturbances, intestinal ischaemia, strenuous physical exercise, sport diet, nutrition
Progress in Nutrition 2015; Vol. 17, N. 4: 317-313 © Mattioli 1885
Original article
Background
e prevalence of gastrointestinal disturbances
(GIDs) during sports practice for athletes, such as
long-distance runners, triathletes, and athletes in-
volved in other types of wearing or long-lasting ex-
ercise is high (1-4). Sports requiring a short but very
strenuous exertion can lead to diverse intestinal distur-
bances such as gastroesophageal reflux GER (2,3,5,6).
Marathon runners, for example, have long been stud-
ied by sport clinicians due to the frequency with which
these athletes report disturbances related to their sports
practice, with a prevalence of up to 50% (7,8). While
some studies are focused on occult bleeding or bleeding
which is sometimes overt, other studies investigated dif-
ferent symptoms and disturbances, like those in Table 1.
Although in some athletes symptoms are also present
during training, those symptoms tend to increase in
frequency and severity during competition due to the
longer length and higher intensity of the physical stress
that the athletes are exposed to.
Among athletes playing long-range strenuous
sports, dehydration and gastric emptying (GE) delay
are the most frequent causes for gastrointestinal (GI)
complaints, and gut ischaemia is the main cause for
their nausea, vomiting, abdominal pain, and diarrhea
(with blood traces) (9).
e cause for these changes in the normal physi-
ology of the gastrointestinal tract is mainly due to
reduced blood circulation (and consequently oxygen
and nutrients) to the internal organs because of higher
energy requirements by muscles, induced by athletic
effort. In humans, during maximal exercise, blood flow
to the gut is reduced by about 80% (7,10).
is condition of relative ischaemia is the most
probable cause for a well-documented alteration of in-
Table 1. Various gastrointestinal symptoms during/after strenu-
ous and continuous exercise
Upper GI Tract Lower GI Tract
Gastric emptying (GE) delay Abdominal pain
Gastroesophageal reflux (GER) Bloating/borborygmus/
gas problems
Heartburn Diarrhea
Dizziness/nausea/vomiting Blood in the stools
Eructation Stitch in right/left side
N. Sponsiello, S. Belgeri, R. Conte, D. Carandini, M. Salamone
318
testinal permeability, inducing severe metabolic stress
in athletes (11,12).
It is reasonable to think that acute GI symptoms
can be more frequent and severe in athletes whose in-
testinal function is less stable, even in the absence of
intestinal diseases.
A serious gut underperfusion often leads to
shock-induced mucosal damage associated with inva-
sion by Gram-negative intestinal bacteria and/or their
constituents (endotoxins) into the blood circulation.
In a specific clinical trial, elevated plasma endo-
toxin concentrations were found in 81% of ultramara-
thoners (90 km-race), with 2% of them exhibiting ex-
tremely high values (13).
Additionally, any factors limiting sweating, such
as a hot and humid environment and/or dehydration,
has profound effects on muscle glycogen depletion and
increases the risk for heatstroke.
Apart from mucosal damage and enhanced per-
meability, a serious gut underperfusion causes blood
loss, microbiota invasion (endotoxemia) and food-
born allergen absorption (with anaphylaxis) (9).
Anaphylaxis is observed during or soon after ex-
ercise, more often when the latter is preceded by the
intake of food-born allergen (14).
In 2000, A.E. Jeukendrup hypothesized that the
gastrointestinal disturbances (GIDs) observed during
and after ultra-endurance exercise could be related to
transition(passage or absorption) of endotoxins [li-
popolysaccharide (LPS)] into circulation in associa-
tion with cytokine production (15).
In that study, performed after a race involving tri-
athletes, an elevation of the reactive C protein (CRP)
was found.
e author concluded that LPS does enter into
circulation after an ultra-endurance exercise, and may,
together with muscle damage, be responsible for an in-
creased cytokine response, and hence GI complaints in
these athletes (15).
GI tract disturbances last days or even weeks in
athletes undergoing strenuous and continuous physical
stress, albeit running (even long distances) may actu-
ally have a therapeutical effect on mild gastrointestinal
problems and IBS (16).
Nutritional practices can correlate with GI com-
plaints. Athletes are generally warned against the risks
of overhydration, and an excessive use of beverages
with a very high osmolarity is not recommended (17).
Gastric emptying (GE) is thought to be negative-
ly affected when the intensity of exercise exceeds 70%
of VO2max, and this has been significantly associated
with increased exercise-induced nausea (18).
The study
is study has been designed to ascertain if a mix
of nutrients formulated to maintain and restore bal-
ance of the gastrointestinal barrier can:
a) (Primary objective) bring general and gastrointestinal
benefits to athletes who train for endurance races;
b) (Secondary objective) reduce the gastrointestinal
effects induced by physical stress, and the conse-
quent pulling out of the race, compared to athletes
not following the treatment.
Achievement of objectives has been measured
through 3 questionnaires specifically formulated and
administered based on this time-frame:
• 4 weeks before the endurance race (Form 1);
• At the end of training period, just before the race
(Form 2);
• At the end of the race (Form 3, and Form 3bis as a
control).
Fifty out of 705 athletes were enrolled at “Tor Des
Géants 2013.” Joining was voluntary, and there was no
selection criteria. As a control (for Objective 2), a ques-
tionnaire (Form 3bis) administered by organizers of the
race (“VDA Trailers”), and sent to all athletes has been
used. In this questionnaire, the reason for pulling out of
the race was asked.
e 50 enrolled athletes followed a supplemen-
tary plan with Nutrimonium at a dose of one portion/
day starting 30 days before the race. e same dose was
also used during the race. No changes to the athletes’ diet
was proposed. During the race, athletes ate/drank the
following: water; food; hydrating substances (with the
exception of those substances that have an effect on the
gut, like probiotics and prebiotics). Some athletes took
supplements and nonsteroidal anti-inflammatory drugs
(NSAIDs).
e following general nutritional indications were
provided to both groups throughout the race:
• During strenuous exercise, it is recommended to
Prevention of acute GI disturbances with a functional food formulation designed 319
drink 0.5 L/hour of water or low-osmolarity sports
drink.
•Itisrecommendedtodrinkbeveragescontainingso-
dium and carbohydrate (CHO) (<10%).
•Glucoseandfructosesourcesshouldbeconsumedto
increase exogenous oxidation of CHO (19).
Tested formulation: Nutrimonium®
e tested product is a base functional food con-
taining nutrients with the composition reported in Ta-
ble 2.
e product is in the form of a powder to be
reconstituted with water. e daily dose used in the
study is equal to one portion, i.e. 11 grams of powder
(1 sachet). Nutrimonium provides no calorie intake.
It is sweetened with sugars from Stevia rebaudiana.
Materials and Methods
The race: the “Tor Des Géants” (TdG)
e “Tor Des Géants” is an ultra trail race of
330 kilometers, and a positive difference in altitude of
24,000 meters. is race requires continuous physi-
cal exertion for most of the 5-6 days (and nights) that
are necessary to complete the course. Athletes have to
spend their time doing physical activity for most of the
time, thus reducing to a minimum sleep and time for
personal care and feeding. 705 athletes started the race.
e first athlete completed the course in 75 hours.
Maximum expected time was 150 hours. Seven “life
bases” and many supply points were available along the
course, where food and beverages could be found.
Samples and data observed with 1st questionnaire
50 healthy adult athletes were enrolled, 44 men
and 6 women. During the first 2 weeks of training,
3 athletes had to interrupt it and withdraw from the
study and pull out of the race due to injuries (n. 2), and
articular problems (n. 1).
us, in the first part of the study, the first question-
naire has been filled in by 47 athletes, with an average
weight of 72.1 Kg, and a BMI of 23.15, which is higher,
on average, compared to shorter races like marathons.
87% of the athletes reported regular bowel move-
ments, and only 6.4% reported frequent diarrhea, or
constipation (4.3%). Symptoms like abdominal swell-
ing were reported by 28.3% of cases.
91% of athletes reported experiencing gastroin-
testinal disturbances during races in the last 2 years,
and 65.9% of athletes said they had to pull out of a race
on at least one occasion due to these problems.
Athletes taking part in the study followed no par-
ticular diet in 81.1% of cases.
Table 2. Nutrimonium® composition (per 1 sachet/11 g - RI*)
Oligofructose-enriched inulin 1500 mg
Lactobacillus acidophilus NCFM
(9 billion alive and viable bacteria)
Bifidobacterium lactis Bi-07
(1 billion alive and viable bacteria)
L-Glutamine 1500 mg
Vitamin A 600 μg - 75%
Vitamin B1 0,825 mg - 75%
Vitamin B2 1.05 mg - 75%
Vitamin B3 12 mg - 75%
Vitamin B5 4.5 mg - 75%
Vitamin B6 1.05 mg - 75%
Vitamin B12 1.88 μg - 75%
Vitamin C 60 mg - 75%
Vitamin D 7.50 μg - 150%
Vitamin E 9 mg - 75%
Biotin 37.5 μg - 75%
Folic acid 100 μg - 50%
Calcium bisglycinate 200 mg - 25%
Chromium picolinate 30 μg - 75%
Iodine 112.5 μg - 75%
Magnesium bisglycinate 93.75 mg - 25%
Manganese citrate 1.50 mg - 75%
Molybdenum 37.5 μg - 75%
Selenium (selenomethionine) 41.25 μg - 75%
Zinc citrate 7.50 mg - 75%
Curcume extract
(95% of which is curcumin) 30 mg
Alpha lipoic acid 75 mg
Green tea extract
(30% of which are polyphenols) 30 mg
*%RI = % Reference Intake (EU)
In admixture with: maltodextrins, flavors, citric acid, silicon dioxide, potas-
sium chloride, xanthane, cellulose gum, carrageenin, steviol glycosides
N. Sponsiello, S. Belgeri, R. Conte, D. Carandini, M. Salamone
320
4 athletes followed an hyperproteic diet; 2 ath-
letes followed a gluten-free diet; and 1 athlete followed
a vegetarian diet. 78.7% of athletes stated they used
supplements while training. Among them, mineral
salts (83%). Supplement use was higher during the
race (83.0%), mainly for mineral salts and protein bars.
4.2% of athletes said they took drugs before the
race to prevent gastrointestinal disturbances.
Global judgment on quality of life was very good
(these are healthy individuals), with values between 6
and 10 (mean: 8.1).
After training: results of 2nd questionnaire
After 30 days, and soon before the race, the data
collected through the 2nd questionnaire, administered
at the end of the 30-day treatment period with Nutri-
monium, can be observed.
e mean weight of the athletes changed to 70.9
Kg, with a mean reduction of 1.2 Kg.
Athletes stating to have regular bowel movements
changed to 95.7% compared to 87.0% in the previous
month (Fig. 1).
Frequency of abdominal swelling lowered from
28.3% to 17.0% (Fig. 2). Still 4 athletes reported fre-
quent diarrhea (8.5%).
74.5% of athletes stated they did not have gastroin-
testinal disturbances during training.
Compliance to the treatment with Nutrimonium
was very good. 91.3% of athletes took the product as
suggested by the protocol.
51.1% of athletes noticed benefits compared to
previous month (Fig. 4).
e most reported benefits were increased resist-
ance (8/47) and better intestinal health (5/47). Other 5
athletes said they had more than one benefit.
Nutrimonium was excellently tolerated in 85.1%
of cases without unwanted effects. 2 athletes reported
“abdominal swelling” as an unwanted effect; 1 athlete
reported “nausea”.
At the end of training period, 14,9% of athletes
suspended treatment due to the absence of benefits
(n=3), or because of unwanted effects (n=2).
At the end of training period, judgment on quality
of life increased to 8.4, i.e. 3.7% more than at the start
of the treatment.
The race: results of 3rd questionnaire
Taking Nutrimonium during the race was prac-
tically difficult. Runners could access their bags only
during pauses at the “life bases” located along the
course at a distance of 40-50 Km apart.
Figure 3. GI disturbances and dropouts due to GI problems
in competitions of previous 2 years
Figure 1. Gut habits regularity
Figure 2. Bloating
Prevention of acute GI disturbances with a functional food formulation designed 321
Despite these difficulties, 36 out of 47 enrolled
athletes took the product even during the race.
At the race’s end, the mean weight of the athletes
was 68.7 Kg, with a mean reduction of 2.2 Kg (3.1%).
ree athletes reported they had severe gastrointesti-
nal disturbances during the race, which led to pulling
out of the race in one case.
21.4% of athletes had some gastrointestinal prob-
lem during the competition (Fig. 5) such as diarrhea,
abdominal pain, abdominal swelling, or slowdown of
digestion during the race.
Use of NSAID’s or pain killers during the com-
petition is very frequent (54.8%) to fight joint pain
arising from overstimulation of the muscoloscheletal
apparatus.
Joint pain/articular problems was the first cause
of pull out from previous edition of competition: Tor
des Geants 2013.
58.5% of athletes taking Nutrimonium during the
race noticed benefits compared to previous races. In
particular, more power and resistance (n = 9); better
gastrointestinal health, or less gastrointestinal symp-
toms (n=9). Six athletes said they had more than one
benefit.
Nutrimonium was also well tolerated during the
race by 90.2% of athletes. Two cases of unwanted ef-
fects (one case of gastric pyrosis and one case of ab-
dominal swelling) were reported.
In the treatment group, 23 athletes (48.9%) com-
pleted the race, and 24 (51.1%) pulled out.
e most common cause for quitting were articular
problems (n =13). Only one athlete’s quitting was due to
gastrointestinal disturbances.
Figure 5. Competitions
Figure 4. Benefits and compliance
N. Sponsiello, S. Belgeri, R. Conte, D. Carandini, M. Salamone
322
The organizers’ control questionnaire (Form 3bis)
e organizers of the race sent a multiple-choice
technical questionnaire to all participants. Questions
included the cause for pulling out of the race.
140 Italian athletes sent their answers.
52 of these athletes were forced to quit, 6 of them
because of gastrointestinal problems (11.5%).
Discussion
Gastrointestinal disturbances (GIDs) are very
common during endurance races, especially in running
races. Although they are not the first cause for quitting
the race, GIDs entail discomfort and effects leading to a
reduction in performance and deprive one of the pleas-
ure of completing the race. e hypothesis supporting
this work is related to a likely change in intestinal wall
function, which is induced by intermittent blood per-
fusion of digestive tract. Our aim was not to interfere
with this specific aspect, but rather to reduce its effects
through a mix of components with a synergistic func-
tion.
As it is a complex product with more significant
chronic effects than acute ones, it was necessary to check
for the occurrence of any changes in intestinal function
during the previous weeks, as well. Bowel movement
regularity is certainly one of the most significant mark-
ers. Checking for improvements (as a percentage) in
subjects complaining of disturbances proves the positive
effect of the product.
e mean compliance to protocol was high. We
believe that if athletes hadn’t had good sensations, drop-
out would have been higher. e absence of adverse ef-
fects should be noted, both chronically and during the
race. We consider the reported good sensations to be
significant.
Of particular interest are the reasons for which
treated subjects pulled out of the race: Only 1 subject
reported GIDs as the cause, while GIDs were definitely
more frequent in control subjects.
Weight loss after ultra-endurance exertion was
considered acceptable if less or equal to 2% (20).
Weight loss is due to a reduced water content in almost
all cases. However, we must also consider that the ma-
jority of data in the literature does not relate to races
with a length equivalent to the TdG. An observational
work on a 100-mile race reports data very similar to
ours (21). It is also likely that a loss of cellular mass
occurs (both in adipose and muscle tissues) over sev-
eral days of race. Moreover, data exists concerning the
likelihood that water content increases due to edemas
formed (22). Given this preamble, the evaluation of
weight loss is very complex. No data on body weight
can be discussed as we did not monitor the volunteers’
caloric intake.
Rules regarding the physiology of exercise cannot
be changed, nor did we want to do that. Muscles need
blood, and enteric circulation provides it. However, we
must find a way so that those whose sport objectives are
very high can find ways to train and adapt every organ
to the type of exercise they practice. Feeling good af-
ter the practice of movement, even if very intense, still
remains one of the main goals of promoting physical
exercise, and also a duty for every instructor.
Evaluation of energy, water and mineral consumption
during the race
e race called “Tor Des Géants” can be consid-
ered one of the hardest races in the world as it requires
intense exertion for more than 21 hours per day for 3-5
days.
We estimated that athletes spent about 10,000-
12,000 Kilocalories per day. In these conditions, the
water-salt balance can also be a determining factor, and
important problems may arise both in the case of dehy-
dration and hyperhydration.
e dramatic reduction in sleeping hours leads to
alterations in attention in many athletes, which often
can result in hallucinations.
Possible insights
is study did not allow for data collection regard-
ing the role of diet versus general state of health, par-
ticularly as a possible determining factor for the gastro-
intestinal disturbances mentioned above. In the future,
it would be useful to compare a group with controlled
feeding and supplements versus a control free-feeding
group with or without supplements.
Prevention of acute GI disturbances with a functional food formulation designed 323
Conclusions
e problem of preventing gastrointestinal distur-
bances is addressed for the first time through supple-
ments with a mix of nutrients in athletes undergoing
strenuous and continuous training and an endurance
race.
51.1% of the athletes who followed the treatment
reported one or more benefits, including more power
and resistance and better gastrointestinal health. At the
end of the training period, judgment on the quality of
life increased to 8.4, i.e. 3.7% more compared to previ-
ous month.
Bowel movement regularity increased from 87.0%
to 95.7%.
Even if not all of athletes took Nutrimonium on
a regular basis during the race, the number of athletes
pulling out of the race due to gastrointestinal problems
was 4.2% (1/24) in the treatment group compared to
11.3% (6/52) in the control group. Nutrimonium was
well tolerated both during training (85.1% of athletes)
and the race (90.2%).
References
1. Simren M: Physical activity and the gastrointestinal tract.
Eur J Gastroenterol Hepatol 2002, 14:1053-1056.
2. Simons SM, Kennedy RG. Gastrointestinal problems in run-
ners. Curr Sport Med Rep. 2004,3:112-116.
3. Riddoch C, Trinick T: Gastrointestinal disturbances in mara-
thon runners. Br J Sports Med 1988, 22(2):71-74
4. Rehrer NJ, Brouns F, Beckers EJ, Frey WO, Villiger B, Rid-
doch CJ,Menheere PP, Saris WH: Physiological changes and
gastro-intestinal symptoms as a result of ultra-endurance
running. Eur J Appl Physiol Occup Physiol 1992, 64:1-8
5. Collings KL et al.: Esophageal reflux in conditioned runners,
cyclists and weightlifters. Med Sci Sport Exerc. 2003,35:730-
735.
6. Parmelee-Peters K, Moeller JL. Gastroesophageal reflux in
athletes. Curr Sport Med Rep. 2004, 3:107-111
7. Morton DP: Factors influencing exercise related transient ab-
dominal pain. Med Sci Sport Exerc. 2002, 34:745-749.
8. Sanchez LD, Corwell B, Berkoff D: Medical problems of
marathon runners. Am J Emerg Med 2006, 24(5):608-615
9. De Oliveira EP, Burini RC: e impact of physical exercise
on the gastrointestinal tract. Curr Opin Clin Nutr Metab
Care 2009, 12(5):533-538.
10. Clausen, J. P. (1977) Effect of physical training on cardio-
vascular adjustments to exercise in man. Physiol. Rev. 57,
779-815
11. Peters HP, Bos M, Seebregts L, Akkermans LM, van Berge
Henegouwen GP, Bol E, Mosterd WL, de Vries WR: Gas-
trointestinal symptoms in longdistance runners, cyclists, and
triathletes: prevalence, medication, and etiology. Am J Gas-
troenterol 1999, 94(6):1570-1581.
12. éktedalen, O., Lunde, O. C., Opstad, P. K., Aabakken, L.
and Kvernebo, K. (1992) Changes in gastro-intestinal mu-
cose after long-distance running. Scand. J. Gastroenterol.
27, 270-274
13. Brock-Utne JG, Gaffin SL, Wells MT, Gathiram P, Sohar
E, James MF, Morrell DF, Norman RJ: Endotoxaemia in
exhausted runners after a longdistance race. S Afr Med J
1988, 73:533-536
14. Fujii H, Kambe N, Fujisawa A, Kohno K, Morita E, Miyachi
Y: Fooddependent exercise-induced anaphylaxis induced by
low dose aspirin therapy. Allergol Int 2008, 57:97-98
15. Jeukendrup AE, Vet-Joop K, Sturk A, Stegen JH, Senden J,
Saris WH, Wagenmakers AJ: Relationship between gastro-
intestinal complaints and endotoxaemia, cytokine release
and the acute-phase reaction during and after a long-dis-
tance triathlon in highly trained men. Clin Sci (Lond) 2000,
98:47-55
16. Halvorsen F-A. et al. Gastrointestinal disturbances in mara-
thon runners Br. J. Sports Med., Vol 24, No. 4
17. Rehrer NJ, van Kemenade M, Meester W, Brouns F, Saris
WH: Gastrointestinal complaints in relation to dietary in-
take in triathletes. Int J Sport Nutr 1992, 2:48-59
18. Rehrer NJ, Beckers EJ, Brouns F, ten Hoor F, Saris WH:
Effects of dehydration on gastric emptying and gastrointes-
tinal distress while running. Med Sci Sports Exerc 1990,
22:790-795
19. Moseley L., Jentjens R.L.P.G., Waring R.H., Harris R.M.,
Harding L.K., & Jeukendrup A.E. (2005). Measurement of
exogenous carbohydrate oxidation: a comparison of U-14C
Glucose and U-13C Glucose tracers. Am J of Physiol En-
docrin & Metab, 289(2), E206-11
20. Sawka MN, et al. (2005) Human water needs. Nutr Rev.
Jun; 63 (6pt2): S30-9,
21. Lebus DK, MS, Casazza GA, Hoffman MD, van Loan
MD. 2010 Can changes in body mass and total body water
accurately predict hyponatriemia after a 161-km running
race? Clin J Sport Med 20(3) 193-99
22. Knechtle B, Wirth A, Knechtle P, Rosemann T. 2009 In-
crease of total body water with decrease of body mass while
running 100 km nonstop--formation of edema? Res Q Ex-
erc Sport.2009 Sep;80(3):593-603.
Correspondence:
Dr. Nicola Sponsiello
E-mail: nicola@nicolasponsiello.com
