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Revista Colombia Médica
Universidad del Valle - Facultad de Salud
ISSN: 0120-8322 EISSN: 1657-9534
Vol. 36, Num. 4, 2005, pp. 281-286
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Revista Colombia Médica, Vol. 36, No. 4, Oct-Dec, 2005, pp. 281-286
Sports as a cause of oxidative stress and
hemolysis
El deporte como causa de estrés
oxidativo y hemólisis
Javier F. Bonilla,
M.D.1,
Raúl Narváez, M.D., M.Sc.2, Lilian Chuaire,
M.Sc.3
1. Assistant Professor, School of Rehabilitation and Human Development,
Universidad del Rosario, Bogotá, Colombia. e-mail: jfbonill@urosario.edu.co
2. Principal Professor, Physiology Laboratory Coordinator, Basic Sciences
Institute, School of Medicine, Universidad del Rosario, Bogotá, Colombia.
e-mail: rnarvaez@urosario.edu.co
3. Principal Professor, Basic Sciences Institute,
School of Medicine, Universidad del Rosario, Bogotá, Colombia. e-mail:
lchuaire@urosario.edu.co
Received for publication December 3, 2004
Accepted for publication October
26, 2005
Code Number: rc05066
SUMMARY
More than three decades ago, it was established that anemia, a cause of tissue
oxygenation deficiency, can be caused by exercise. However, this preliminary
relationship really corresponds to an event where the plasma is diluted and
for this
reason the term «sports pseudoanemia» was made. New data relate exercise
from moderated to exhaustive, with blood loss through gastrointestinal and urinary
tracts, as well as erythrocytes rupture by mechanical, osmotic and oxidative
events. Therefore, now the association between chronic exercise and impairment
in erythrocytes number and form is clearer, which is evidence in favor of a true
anemia in sports. In this anemia it is evident the ferropenic etiology. But recent
information opens discussion about whether hemolytic etiology is a co adjuvant
factor to anemia, and on the role of oxidative stress in it. This paper is an
updated review for a relationship between sports and anemia, and for assessing
causes of
ferropenic anemia and for sports hemolysis.
Key words: Anemia; Physiology; Exercise.
RESUMEN
Desde hace más de tres décadas se
estableció que el ejercicio puede producir la anemia, una de las causas
en la deficiencia de oxigenación a los tejidos. Sin
embargo, esta relación preliminar realmente corresponde a un evento donde
el plasma se diluye, razón por la cual no es una verdadera anemia, por
lo que se acuñó el término pseudoanemia del deportista.
La nueva información relaciona el ejercicio, de moderado a exhaustivo,
con la pérdida de
sangre a través de los sistemas gastrointestinal y urinario,
así como con la ruptura de los eritrocitos debida a eventos
mecánicos, osmóticos y oxidativos. Entonces ahora es
más clara la asociación entre el ejercicio
crónico y el deterioro en el número y forma de los
hematíes, lo que constituye evidencia en favor de una verdadera anemia
del deportista, de clara causa ferropénica.
La información reciente abre la discusión acerca de la
etiología hemolítica como factor coadyuvante en la anemia, y acerca
del papel que en ella tiene el estrés
oxidativo. La presente es una revisión actualizada que relaciona el deporte
y la anemia, además de presentar los
orígenes de la anemia ferropénica y de la
hemólisis en deportistas.
Palabras clave: Anemia; Fisiología; Ejercicio.
Anemia could be defined as the status in which the quantity and quality of
circulating erythrocytes is below the normal levels for a determined individual,
according with the reference ranges for hemoglobin (Hb) and erythrocyte count
appropriate to age, sex and sea level as well.
There is a recent number of investigations that inform about changes in the
physiological erythrocyte indices as well as in the erythropoyesis itself after
a physical training session in general, or a high intensity aerobic exercise
(1). This fact leads to postulate the physical exercise as a possible cause
for anemia. From
this it was derived more than three decades ago the term «sportsmen anemia» (2-4)
to define a limit anemic status (borderline) proper for individuals who practice
some physical activity on a regular basis, e.g. athletes (5). Who were found
a hemodilutional effect, which should not be considered as a true anemic condition
but a reologycal adaptation to exercise (6).
Several researches indicate that the frequency of this kind of anemia is similar
in problem groups constituted by athletes, in respect to control groups. Exercise
could affect Hb concentration in an undetermined way, since during and after
the exercise session it is possible to find modifications in its values, for
example due to hemo-concentration or to changes in the individual hydration
grade (7).
A great part of the difficulty to precisely determine whether there is an
anemia due to exercise resides in the existing differences among the researched
population, as well as in the diversity of definitions and etiologies proposed
for the anemia
(8).
When etiology is associated to dilution, we are not dealing with a true anemia.
From this the term pseudo-anemia is derived. Today, when the exercise benefits
are every time more controversial (vgr. sportsman sudden death) (9) and there
exist diverse research in favor or against the physical activity whether it
is regular or occasional (10), it is important to determine whether exercise
is the cause of anemia in the individual, who could be through other etiologies
added to the event associated to dilution. From this perspective, the diagnose
for a true anemia must be done through the evaluation of clinical aspects but
also hematological parameters such as the media corpuscular hemoglobin (CHCM)
which is
not affected by the hemodilution (11).
Whenever the ferropenic etiology is evident, exercise is described as one
of the causes of anemia. It is under discussion how much the hemolitical etiology
contributes to the sports anemia and therefore the role of the oxidative stress
in this
anemia is being better understood.
Ferropenic anemia secondary to exercise. Ferropenic anemia is related to a
decrease in the sportsmen performance (12). It affects particularly to marathonists
and this is the most researched form of anemia (13). Its causes could be the
hemoglobinuria, hematuria, gastrointestinal blood loss and iron loss due to
profuse sweat (14).
Hemoglobinuria. The first report about the hemoglobinuria associated to exercise
dates from 1881, when Fleischer in Jones and Newhouse (15) described the presence
of obscure urine in a young soldier after his participation in a march, and
he named it as the marching hemoglobinuria. Hemoglobinuria, sometimes associated
to hematuria, could promote an anemic condition in competitive athletes (15)
specially those running long distances (16). This anemic condition has been
related to hemolysis associated to exercise and to consequent hypohaptoglobinemia
and plasmatic Hb increase (17). There is much evidence that hemoglobinuria
could be most common than believed, although it seems to be self-limited and
benign
(18).
Hematuria. Hematuria is documented from contact exercise (football or box)
as well as in non-contact ones (swimming or soaking). It could be macro or
microscopic. It is frequent, self-limited and benign, since it disappears 48
to 72 hours after exercise (18). It could be related or not to gall bladder
and/or renal trauma. Whenever it is not traumatic, it is associated with glomerular
ischemia due to the constriction of the renal and splenic vessels or it could
also be due to an increase in the filtration pressure secondary to the efferent
arterioles constriction. The severity of the hematuria is proportional to the
intensity and duration of exercise (19) and could course with dehydration,
myoglobinuria and lipid peroxidation in erythrocytes (15,20).
Gastrointestinal blood loss. The digestive blood loss is frequent after a
prolonged exercise (21). In marathon athletes, it is present with a frequency
of 8% to 30%, not associated to inflammation nor with gastric blood loss (22)
and apparently it is independent from age, career time, abdominal symptoms,
and recent ingestion of vitamin C or acetylsalicylic acid (23). The digestive
blood loss related to the intensity of exercise could induce a decrease in
the circulating erythrocytes and therefore increase the
iron loss (24).
Iron loss for profuse sweat. This form of iron loss has been evaluated in
several researches, during and after an exercise session, in trained individuals
and non-trained ones as well. Results indicate that this loss depends directly
on the amount of sweat, since this is higher in prolonged exercise under high
temperatures. There is not a significant difference between women and men.
The possible severity of this loss depends on the sportsmen iron reserve (iron
status) (25,26).
DOES HEMOLYSIS CONTRIBUTE TO SPORTS
ANEMIA?
Several authors have described a significant increase in the destruction of
the erythrocytes after intense physical exercise (27). In 1943 Gilligan et
al. (17) evaluated the hemolysis associated with intense exercise when determined
the plasmatic hemoglobinemia and the hemoglobinuria in marathon athletes. The
most affected with this condition are athletes, specially those elite athletes
who apparently constitute the most susceptible population. The hemolysis intensity
depends on the race distance (27). Also it has been found hemolysis associated
with sports such as swimming (28), soaking, triathlon and aerobic dance (29)
as well as in non-competitive races and in rigorous military training (30).
One on the causes for this hemolysis is the fact that after a strong exercise
the erythrocytes are more susceptible to stress, whether of mechanical, oxidative
or osmotic type (31). The oxidative stress could also alter the ionic homeostasis
and facilitate the cellular dehydration. These changes decrease the deformability
of the red cell
thus impeding its passing through the micro-circulation (32).
Telford et al. (33) informed about the large ranges in the increase of the
plasmatic Hb concentration and the haptoglobine (Hp) decrease in amateur athletes
and cyclists who were
taken to the maximum oxygen (VO2max) consumption and to the same exercise
intensity as well. These facts lead to assume the occurrence of hemolysis in
both sportsmen groups. The free Hb increases up to 85+35 Hb mg per each plasma
liter, with a higher and a more persistent increase in the Hb plasmatic concentration
in the
athletes.
On the other side, recent researches suggest the possible hemolysis in sportsmen
(34) caused by mechanical effects since they strike erythrocytes and promotes
their destruction. The same occurs with long-distance runners when hemolysis
occurs as a consequence of the repeated foot impact (footstrike) over the surface
(33).
What is the reason why some sportsmen present a higher grade of hemolysis
than other, considering that they are under the same conditions of intensity
and exercise length? It is necessary to think that hemolysis during and after
exercise could be the result of running long distances where erythrocytes are
stroke, but it also result from other mechanisms such as the oxidative stress
(28,33).
Sportsmen hemolysis caused by oxidative stress. Oxidative stress is described
as the event in which the free radicals are over the systemic mechanisms of
the antioxidative defense (35). In 1978 Dillard et al. (36) were the first
in demonstrating that
physical exercise leads to a lipid peroxidation increase.
It is estimated that at rest, 2% to 5% of electrons flow of the respiratory
chain escapes to form reactive oxygen species (37) (ROS), such as peroxide
(O2-), hydrogen peroxide
(H2O2), hydroxyl (OH-) and those associated with nitric
oxide
(NO) (38).
The mitochondria is a source of ROS, although it is not necessarily the most
important (at least in vitrol) since
during exercise it increases the O2 tissue consumption range. There
is an experimental indicating evidence of increase in the ROS production, as
well as oxidative stress and tissue damage associated with exercise, whether
exhaustive and severe (39), or moderate (40). During exhaustive exercise, the
muscle oxygen consumption increases 100 to 200 times if compared to the one under
rest status (41). This induces an electron flow increase through the mitochondrial
respiratory chain, which at the same time results in an increase of ROS production
(38). It has been determined recently that mitochondrion also generate NO, which
could be a part of the free radicals total production during exercise. When NO
reacts with
O2, it forms peroxynitrite (ONOO-), a powerful oxidant. This reaction
is
believed as the main via to generate reactive nitrogen species (RNS)
(42).
Oxidative stress could occur in individuals whether or not adapted to exercise,
thus making them susceptible to present injury in their enzymatic systems,
as well as in lipids and
membrane receptors and also in their ADN (42,43).
Now, the ROS and RNS actions could occur at the end of the exercise session
or hours after it. Available information associates exercise with ROS and RNS
production through three
evidences related between them, such as:
- The free radicals production is muscle, liver, heart and blood.
- The increase in the biomarkers of oxidative damage, such as protein
carbonyls and substances reactive to thiobarbituric acid44, and the
increase in the exhaled pentane levels, which is a possible result of the
lipid oxidative
damage (36).
- The decrease in the antioxidant enzymatic and non-enzymatic levels
in heart, blood (45), brain and muscle (46).
Another generating source of ROS is the xanthine-oxidase (XO) via which contributes
to the H2O2 tissue generation with high xanthine and
hypoxanthine concentrations. Tissue hypoxia, through the XO (43) via could
generate oxidative stress during exercise (47). This occurs also after events
of ischemia-reperfusion
in organs such as heart (48).
XO activation is produced during exhausting exercise thus allowing ROS generation
in different tissues (42,49). For example, in the skeletal muscle the hypo-xanthine
is liberated to blood, thus the XO enzyme is activated (50). Radak et al. (51)
demonstrated that the XO via is also committed in the
O2 generation.
The third source of ROS is the peroxisomes. In physiological conditions these
organelles produce H2O2 but not peroxide. Peroxisomal
oxidation of the fat acids is an important source of
H2O2. Since fat acids are a source of energy for heart
and for skeletal muscle during exhaustive exercise, it is probable that peroxisomes
contributes to the oxidative stress in sportsmen
(38).
A fourth source of ROS is the polymorphonuclears leukocytes (PMN). When neutrophile
PMN are
activated (respiratory burst) they liberate O2-. Therefore, if does
exist tissue damage caused by exhaustive exercise, the subsequent neutrophile
activation becomes a source of ROS (38,52). These activated cells could cause
lipid peroxidation in closer cells, and in erythrocytes (53), since their products
are able to cross the cellular membrane and produce Hb oxidation (54) which will
initiate the hemolysis process. Moreover, the ROS oxidizing action over low density
lipoproteins (LDL) (56) and over the lipids of the erythrocyte membrane are associated
with hemolysis (53,57).
The neutrophile PMN could infiltrate the muscle tissue damaged by high-density
exercise. When this occurs, the
O2- generated through oxidase NADPH associated with the membrane,
reacts
and leads to H2O2 formation. This last has become a
hipochlorosus acid (HOCl) for a hemoproteic myeloperoxidase secreted by neutrophiles
and monocytes.
HOCl is an inflammatory mediator, powerful oxidant and chlorinate, since
at the same time it generates other reactive
metabolites such as nitryle chloride (NO2Cl) in presence of nitrite.
Nitrite could become, through the myeloperoxidase and
H2O2, the radical nitrogen dioxide (NO2)
that facilitates the formation of other high injuring substances (42). Since
neutrophiles
infiltration in the tissue injured by exercise is secondary to production
and liberation of proinflammatories, this via may not be the first source
of ROS
production during exercise. However, it could certainly serve as an important
source during the recovery period after exhaustive exercise (58). A fifth
source of ROS is the catecholamines, although their contribution to the free
radicals
has not been quantified (38). For example, it has been proposed that in oxidative
lesion of the myocardial ischemia-reperfusion, it occurs the epinephrine
autooxidation in adrenochrome, associated with
O2 formation.
There has been established that the iron and the hemo group of hemoglobin
and myoglobin are potential sources of ROS (42), but it is not clear yet how
much they participate in the oxidative stress during or after exhaustive exercise
(59).
Several researches in vitrol discard mitochondria as the main producer of ROS
during exercise, since they sustain that these Hb-Mb system is not only capable
to generate it but also to increase the reactivity of those produced by other
via.
Within the radicals generated there is 2-, ferryl iron
(Fe+4=2-) and free radicals joined with proteins (59).
The Hb-Mb system causes injuries in different ways. Thus, following Hb liberation
to intravascular space, as a consequence of hemolysis, there is the formation
of Hp/Hb complex. But an intense hemolysis saturates the Hp capability to alloy
Hb, which takes Hb to remain free in plasma (60). In the same way, Mb could
be free in plasma due to processes such as the rhabdomyolysis, usually associated
with exhaustive exercise. When free Hb and Mb are oxidized, they become citotoxic
substances and could injury the endothelia (atherosclerosis, vasculitis) and
also the erythrocyte
itself (intravascular hemolysis) (61).
Hb and Mb oxidation is associated with the ROS liberated from activated leukocytes,
during exhaustive exercise and hypoxia. The methemyoglobin (metHb) and metmyoglobin
(metMb) thus generated, as well as their derivatives are capable to produce
more ROS, besides lipid peroxidation, with formation of hydroperoxides (59,62).
Other researchers have found that hemo group is related with membrane protein
oxidation and with formation of surface antigens in senescent red blood cells
(63).
Therefore there are established direct and indirect injury mechanisms from
Hb and Mb and from their derivatives. One example of the direct one is the
primary cytolysis caused by ROS from the type ferryl iron. As an example of
indirect mechanisms is the sensibilization to the damage caused by hydroperoxides
from the oxidizing LDL type. These mechanisms receive feedback in a way that
origins vicious circles: the exercise is a hypoxemic process that generates
hemolysis and thus liberates Hb and Mb and their derivatives, which facilitates
more hemolysis and more hypoxemia
(59).
There exist two control ways that limit the action of the free hemo: the cellular
via in which Hp and hemopexin take part and the intracellular one, where hemooxygenase
and ferritin participate. These ways are rebased with a defect in the control
ways, or if there is an excessive elevation of the free hemo
(61).
CONCLUSIONS
Sportsmen pseudoanemia is related with a plasma expansion. In individuals
who practice frequent aerobic sport activity it could coexist associated events
such hematuria, gastrointestinal blood loss, as well as an increase in the
intravascular hemolysis. These factors link exercise with the deterioration
of corporal iron reserve and the erythrocyte number and morphology. Likewise
there are foreseen much more etiological possibilities not only of entities
like anemia, but of a great number of other diseases related to exhaustive
and competitive exercise with
damaging responses to the organism.
It is necessary to deeply study the reasons why some sportsmen present higher
grades of hemolysis than others, even when they are submitted to similar conditions
of intensity and work terms. For this, it must be considered that hemolysis
in exercise could result not only from running long distances where erythrocytes
are stroke, but also from other mechanisms such as the oxidative stress. To
thoroughly understand the mechanisms of action of the oxidative stress and
the mechanisms of response of the erythrocyte constitutes an important challenge
within the sports physiological
field.
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