Simons Pap Final

GI problems in distance running International SportMed Journal, Vol.6 No.
3, 2005,
pp. 162-170 http://www.ismj.com

ISMJ
International SportMed Journal

Review article
Gastrointestinal problems in distance running

*
Dr Stephen M Simons, MD, FACSM, Dr Gregory G Shaskan, MD
Saint J oseph Regional Medical Center, South Bend, IN 46545, USA

Abstract
This article reviews the literature of gastrointestinal (GI) problems in runners. These problems
commonly affect runners and some believe that they can hamper performance. Many
physiologic processes, including the interplay of decreased transit time, absorptive effects,
hormonal changes, and endotoxins breaching the bowel wall contribute to an incomplete
understanding of the physiology behind the pathology. Upper GI pathology, such as
gastroesophageal reflux disease (GERD), nausea, and vomiting, can detract from the
pleasurable aspects of running, while gastritis, hepatitis and pancreatitis can threaten the health
of the athlete. Lower GI pathology, such as diarrhoea and colitis, can similarly taint the runners
experience. The authors examine various pathologies suspected of contributing to runners
anaemia, the side stitch, and the effect of running on previous GI pathology. Also discussed are
important elements of history, physical examination, and treatments. Keywords:
gastrointestinal, exercise, running, runners, GI

Dr Stephen M Simons, MD, FACSM
Dr Simons is the Director of Sports Medicine at the Saint J oseph Regional Medical Center,
South Bend, IN, USA. He is also the Co-Director of the South Bend Sports Medicine
Fellowship. Dr Simons is involved exclusively in clinical medicine, and his medical practice
focuses on all aspects of running.

He was a Volunteer Physician, United States Olympic Committee Athens Summer Olympic
Games, Pan American Games, and a Team Physician, St. Marys College, Bethel College,
USA. He is a Volunteer Physician at the University of Notre Dame.

Dr Gregory G Shaskan, MD
Dr Shaskan is a Resident at the Saint J oseph Regional Medical Center, South Bend, IN, USA.
He works with Dr Simons in a medical practice that focuses on all aspects of running.
Contact details:
Email: shaskang@sjrmc.com

Official Journal of FIMS (International Federation of Sports Medicine)

162
*
Corresponding author. Address at the end of text.
GI problems in distance running International SportMed Journal, Vol.6 No.3, 2005,
Introduction
The most notable and often quoted sports-
related gastrointestinal (GI) event came
from Derek Clayton after his world record
setting marathon in 1979, Two hours later
the elation had worn off, I was urinating
quite large clots of blood, and I was
vomiting black mucous and had black
diarrhea.
1
.

While, thankfully, not all runners will suffer
Claytons fate, different studies show that
GI disturbances afflict between 30-83% of
runners
2
. In one study, up to 29% of
those with complaints believed that their GI
pathology negatively affected their
performance
3
. Women runners seem to
be more affected than men
4
. Runners
reported more lower- than upper GI
complaints, which is in contrast to the
more even distribution of GI symptoms in
cyclists and triathletes
5
.

Pathophysiology
While GI symptoms seem rampant, their
pathophysiology is not fully understood.
To date, contributing theories mainly focus
on the mechanical agitation of the gut, fluid
shifts, decreased splanchnic blood flow,
dehydration, increased sympathetic and
parasympathetic tone, endotoxaemia,
changes in bowel transit time, hormone
shifts, and autoimmune changes.
However, none of these adequately
explain the full range of GI pathology
2
.

The mechanical forces during running
assuredly play a part in GI pathology.
Peters et al. show that runners exhibit
more GI symptoms than cyclists
5
. This
could be as a result of running, which
imposes approximately twice the
acceleration/deceleration forces rendered
by cycling at a similar workload
6
. It might
be concluded that a semi-solid stool
liquefies from the churning effect caused
by decelerating the colon contents when
the foot strikes the ground.


162
Exercise-induced fluid imbalances are
likely to contribute to GI pathology in
runners. Rapid fluid shifts into the colon
may cause irritability and cramping
7
.
Intense exercise can decrease splanchnic
flow, while dehydration further reduces the
intra-abdominal perfusion. One study
showed that 80% of marathon runners,
losing at least 4% of body weight,
experienced GI problems
8
. A cohort of
ultra-endurance runners studied by Glace
et al.
9
showed that while GI disturbances
could also occur in the absence of
dehydration, most occurred after
prolonged running. Improved fitness
through training reduces the dramatic
blood shift away from the GI tract and
therefore at any given workload, the
greater the fitness level of the runner, the
fewer GI disturbances are experienced
10
.

Researchers have also questioned
whether transit time (i.e. the time it takes
for food to travel through the gut) changes
during distance running, and whether this
has an overall effect on GI symtomotolgy.
Van Nieuwenhoven et al. have found that
GI transit time is longer and permeability
greater in symptomatic runners than
cyclists or asymptomatic runners
11
.
However, Kayaleh et al. refute this
evidence, as their study of athletes,
running 9.6km/hr for one hour, found no
change in transit time
12
.

Changes in intestinal permeability may
have an effect on endotoxaemia. The
gram-negative intestinal floras that
normally inhabit the gut have cell
membranes that contain
lipopolysaccharide (LPS). When LPS is
released into the blood, it is associated
with an increase in cytokines and can lead
to fever and shock. It has been shown that
runners who take a long time to finish a
race have a greater level of endotoxaemia
13
. Furthermore, endotoxaemia and
increased cytokines may lead specifically
to GI pathology
14
. Walsh et al. also
postulate that endotoxin entry into the
portal circulation may lead to grave effects,
such as portal vein thrombosis via a local
hypercoagulable environment
15
.

Several studies implicate chemical and
hormonal disturbances as causes of GI
disturbances in runners. Sorting through
the quagmire of these biochemical
changes is staggering. Predicting the
clinical symptoms associated with each of
these individual changes will prove to be
even more challenging. In one study,
athletes completing a 67km alpine
marathon had elevations of cortisol,
adrenaline, and noradrenaline
16
. GI
symptoms were more closely correlated
with lower post-race cortisol and
noradrenaline levels and elevated post-
race potassium. Causal relationships, of
course, were impossible to confirm.

OConnor et al. believe that the body
meets increased exercise demand by
profoundly elevating several GI hormones
17
. These include vasoactive intestinal
polypeptide (VIP), gastrin, secretin,
pancreatic polypeptide, neurokinin A,
pancreastatin, and motilin. VIP, acting as
a vasodilator, is thought to combat the
splanchnic vasoconstriction.

Interestingly, exercise-induced immune
system changes may also play some role
in the GI pathology of runners. One study
showed that, in mice, CD3+and CD8+cell
apoptosis is increased significantly after
strenuous exercise above that of the
controls
18
. While many of these isolated
physiologic phenomenon peak interest,
their contributions toward a complete
understanding of GI pathology or clinical
symptoms remain unclear.

Upper gastrointestinal tract
Runners suffer a variety of upper GI
complaints, ranging from common
disorders, such as gastroesophageal reflux
disease (GERD), nausea, and vomiting, to
the rare critical disorders, such as acute
hepatitis, omental infarct, and pancreatitis.
The occurrence of these symptoms during
running does not always vary from the
occurrence of these symptoms at rest
19
.

Gastroesophageal reflux disease
(GERD)
As previously mentioned, upper GI
complaints are common in runners. Even
runners without a history of GERD
demonstrate reflux during exercise as
shown by manometry
20
. At levels of 70%
VO
2 max
, lower oesophageal sphincter tone
decreases
21
. As intensity levels of 90%
VO
2 max
induced more reflux, Soffer et al.
have shown that oesophageal contractions
decrease with increasing exercise intensity
22
. Reflux is also associated with belching
during running
23
.

Several studies conflict on whether reflux
occurs more frequently in runners than in
cyclists
24, 25
. In fact, one study of 93
runners shows that runners have
decreased GI symptoms over non-runners
26
. However, as reported rates of GERD
vary with the intensity of the run, it may be
misleading to compare different modes of
exercise without also including
measurements of intensity
16, 9
. Choi et al.
found that fed runners experienced
significantly more reflux as exercise
intensity increased
27
. In Choi et al.s
research, the meal consisted of 8 rice rolls
(660 cal) and water before exercise, and
subjects were seated for 30 minutes
before testing began
27
.

While reflux may contribute to chronic
cough and asthma, Weiner et al. showed
no significant correlation between reflux
and exercise-induced bronchospasm in
asthmatics
28
.

Of clinical importance is the distinction
between exercise-induced GERD and
cardiac pain. Schofield et al. found that
44% of those experiencing exertional
reflux on stress testing also had chest pain
29
. DeMeester et al.
30
found 46% of
patients with anginal symptoms and
normal coronary arteries had reflux on 24-
hour pH monitoring. Exertional pH
monitoring provided improved diagnostic
certainty for non-cardiac chest pain, with
68% of patients showing pathologic reflux,
and 27% having chest pain with an
exercise stress test apparently related to
reflux
31
.

Vomiting and nausea
Many athletes and coaches may still insist
that a workout is not complete till you
puke. Sullivan et al. found that while
runners retch more than non-runners, they
do not vomit more
26
. However, intensity
of running may play a role in whether one
retches or vomits. Eating and the use of

163
non-steroidal anti-inflammatories (NSAIDs)
prior to running increases nausea and
vomiting
9, 32
. A study of those athletes
completing a half Ironman triathlon found
that all who had eaten 30 minutes before
the start of the competition vomited
33
.

Gastritis and stress ulcers
As mentioned, complex GI physiology is
elusive and the definition of the interplay of
the many experimentally demonstrated yet
separate phenomena is still incomplete.
Because mice share roughly 90% of the
genetic material of a human, experimental
mouse models hint at much of the basic
physiology underlying activity-induced
stress ulcers. For instance, it is known
that food deprivation of mice induces
stress ulcers independent of activity
34
.
However, in mice, exercise will increase
ulcers that are already present
35
. Morrow
et al. show that the brain has an effect on
the GI system; specifically, the
centromedial amygdala which plays a
protective role in mediating stress-exercise
ulcers. However, the pathway by which it
does this is unclear
36
. In yet another
study, Doi et al. were able to decrease
stress-exercise ulcers by decreasing
parasympathetic input using either
anticholinergic drugs or truncal vagotomies
37
. Watanabe et al. demonstrate that
circadian rhythms, weight loss, and
exercise level influence the formation of
stress ulcers
38
. Much of this interesting
research might lead one to question
oversimplified physiologic models that do
not take into account the interplay of the
bodys systems.

In humans, increased intensity running
also increases GI permeability; however, a
lack of correlating symptoms caused Pals
et al. to question its clinical significance
39
.
Trials, including one at the 1996 Chicago
Marathon, have varied slightly in their
interpretation as to whether ibuprofen,
aspirin or both have a role in increased GI
permeability
40, 41, 42
. In a study of runners
with anaemia it was found that the majority
had gastric or oesophageal ulcers
43
.
However, there seems to be some good
news for runners, as Cheng et al. showed
that men walking or running more than ten
miles (16km) a week had fewer ulcers than
those who did not
44
.

Hepatitis and pancreatitis
If running is hard on the system,
ultramarathons can wreak havoc.
Ultramarathoners see a transient rise in
many blood chemistry parameters,
especially their hepatic enzymes. Some of
these can be explained by vast fluid shifts,
others to widespread tissue injury. Several
studies have shown significant rises in
total bilirubin (BIL-T), direct bilirubin (BIL-
D), alkaline phosphatase (ALP), aspartate
aminotransferase (AST), alanine
aminotransferase (ALT) and lactate
dehydrogenase (LDH)
45
. Some of these
values can stay elevated for up to seven
days after finishing an ultramarathon
46
.
Plasma enzyme elevations seem to return
more quickly for the experienced and more
highly trained runner
47
. Clearly the
evidence shows that ultramarathons affect
the liver; but the consequences of this are
not fully understood
48
.

It is worth noting case reports that describe
marathoners suffering running-induced
pancreatitis with significant morbidity
49
.
While the aetiology is not understood,
possible causes vary from ischemia to
direct mechanical trauma
50
.

Lower gastrointestinal tract
Lower GI tract symptoms include lower
abdominal cramping, the urge to defecate,
increased bowel frequency, and diarrhoea.
These symptoms can interrupt both
training and competitive runs, as well as
cause awkward social situations
35
.
Studies estimate the frequency of these
symptoms to be between 37-71%
51, 52
.
Such interruptions can prove costly: one
elite marathoner stopped at a service
station at 22 miles (35.2km), returned to
the race and won. However, she
inadvertently trimmed 30 meters off the
42km course, was disqualified, and lost the
US$41000 prize money
52
.

Peters et al.
19
surveyed 606 runners,
cyclists, and triathletes about their last 12
months of activity. Running, either as the
lone activity or as the running portion of

164
the triathlete's training caused a
preponderance of lower GI symptoms
when compared to nearly equal upper- and
lower GI problems in cyclists. Ultra-
endurance activity may show different
patterns of GI disturbance. This is
illustrated in the previously mentioned
study, where Glace et al.
9
followed 19
runners participating in a 160km event.
Half of the participants experienced GI
disturbances. In contrast to previous
studies of events of shorter duration, upper
GI symptoms predominated and occurred
mainly after 88km. The authors speculate
that the slower pace contributed to the
differing GI disturbances in this ultra-
distance event.

Colitis
Like running-induced pancreatitis, acute
colitis following exertion rarely occurs. The
cases reported suggest ischemia as the
cause of the acute colitis
53, 54
. Blood flow
to the GI tract can decrease to 20% of
normal. This sustained reduced blood flow
may then lead to mucosal injury and
necrosis. Exercise intensity and duration
may contribute to higher rates of blood
loss. The watershed areas between
mesenteric arteries are probably the most
vulnerable areas of the bowel subject to GI
ischemic pathology. Mechanical irritation
to the mucosa may also contribute to
injury.

Miscellaneous
Anaemia
Between 8-23% of runners may
experience hemoccult-positive stool
55
.
While the clinical significance of this is
unknown, GI blood loss may contribute to
a macrocytic anaemia commonly known as
runners anaemia
56
. Other suggested
causes include pounding of the feet on the
pavement and hemoglobinuria.

Exercise-related transient abdominal
pain
The side stitch, commonly also known as
cramps, usually affects runners in the right
or left upper quadrant. The pain may also
be referred to the shoulder, possibly
implicating hepatic, splenic, or phrenic
nerve involvement. Many athletes report
some history of exercise-related abdominal
pain, specifically 69% of runners
57
. These
sufferers describe the more severe pain as
sharp and the less severe as a
cramping, aching, or pulling. This
syndrome seems to decrease with
increasing age and training status, but sex
and body mass index do not affect the
frequency
58
. Thus the authors encourage
runners to continue their regimen with the
expectation that the symptoms will
improve.

Of anecdotal interest, rhythmic breathing
techniques seem to help less experienced
runners deal with this affliction. The
runner should inhale during three steps
and exhale on the fourth, leading to a
sequence of exhaling on every other right
foot strike. This provides an alternative
focus of concentration, in addition to
standardising the diaphragmatic interaction
with foot strike.

Running effect on previous GI
conditions
Little evidence exists regarding running
and inflammatory bowel disease or irritable
bowel syndrome. Sedentary patients with
Crohn's disease have been found to
tolerate a low-intensity walking programme
without exacerbating the condition
59
.
However, due to the problems of
dehydration, electrolyte disturbances, and
blood loss during a flare-up of
inflammatory bowel disease, strenuous
running should be avoided
60
. While
women with irritable bowel syndrome are
less likely to be active, those who are more
active report less fatigue
61
.

Treating GI pathology in runners
History and pathology

165
The complete evaluation of GI
disturbances in runners begins with a
thorough history. As with non-athletic GI
complaints, pertinent medications, other
current conditions, past medical history,
family history, and travel should be sought
to explain other possible causes. The
physician should also ask about specific
training schedules and recent changes in
those schedules
62
. In the light of the
continued onslaught of performance
enhancers, physicians should take a
careful dietary history, including a frank
discussion of any oral or parenteral
supplements. The physical examination,
including abdominal inspection, palpation,
and auscultation, may help rule out any
disease not already elicited from the
history.

Investigations, as a rule for
hemodynamically stable, non-critical first
presentations, are generally not
necessary. Recurrent symptoms,
however, require a higher level of
suspicion to rule out other GI pathology.
Choi et al., using endoscopy and
colonoscopy on 16 young competitive
runners, found a high prevalence of
mucosal damage. They suggest
endoscopic techniques before starting
treatment for those athletes who present
with GI symptoms or anaemia
63
. The
physicians judgment concerning each
presenting case is paramount.

Treatment
Todays common wisdom states that the
pre-event meal may not critically assist
performance, but it has the ability to harm
performance. Avoiding foods before
exertion will decrease GI symptoms. In
one study, all athletes eating within 30
minutes of the start of a triathlon vomited
33
. A common sense practice would be to
withhold large meals for at least three
hours before running. What is eaten also
has an effect: the consumption of
carbohydrates increases reflux over
consumption of water
24
.

Aspirin, while not causing symptoms, has
been shown to increase GI permeability,
and the risk of its use should be
considered especially with a previous
history of anaemia
64
. Based on research
undertaken during the 1996 Chicago
Marathon, Smetanka et al. showed that
NSAIDS should also be avoided
40
.

166

Physicians may want to consider
medications for symptomatic relief. Peters
et al. found that the proton pump inhibitor
omeprazole can reduce reflux in runners
65
. Cimetidine, an H
2
blocker, was shown
to decrease nausea and vomiting in
running
66
. A case report showed that H
2

blockers have also stopped running-
induced erosive gastritis
67
. Researchers
have not yet performed equivalent dose-
controlled trials comparing H
2
blockers to
proton pump inhibitors in runners; and as
these trials would be difficult to perform,
physician judgment remains the deciding
factor.

Performance improvement
A small random trial using sodium citrate
against placebo in 3000m runners showed
significantly improved performance times
and increased levels of lactate. However,
use of sodium citrate as an enhancer
would be severely limited due to its high
rate of gastric disturbances
68
.

Conclusions
GI disturbances occur commonly in
runners, their effect ranging from mildly
annoying to critical morbidity. While the
pathophysiology is not completely
understood, common sense preventative
measures and basic GI medications can
lessen the severity of an aggravating
disease. Future performance
enhancements might be improved through
combinations of physiologic and
medication knowledge.

Address for correspondence:
Dr Stephen Simons, 230 E. Day Rd, Suite
150, Mishawaka, IN 46545, USA
Tel.: +1 (574) 247 5678
Fax: +1 (574) 247 5677
Email: simonss@sjrmc.com

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GI problems in distance running International SportMed Journal, Vol.6 No.

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