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Effect of exhaustive exercise on the immune system, measured through complement activation and C-reactive protein Ana Navarro Sanz1, Jesús E. Barruecos Francioni2, Lorenzo Godoy Sánchez3, Antonio Narvaez de Linares2, Juan L Galeas-López2, Ana Robles Rodríguez2, Juan F. Fernández Ortega21Center Sport Medicine. Área de Deporte. Málaga City Hall. Spain.
2ICU. Hospital Universitario Carlos Haya. Málaga. Spain.
3Clinical Laboratory. Hospital Universitario Carlos Haya. Málaga. Spain.
Recibido:
Aceptado:
The infl uence of exercise in the systemic infl ammatory response has been a subject of debate for over ten years. However very
few original studies have analyzed their activation and are practically nonexistent translational studies that have extrapolated
the analysis results to the reality of athletes.
Purpose: We aimed to determine the eff ect of exhaustive exercise on two known infl ammatory markers, the complement
system and C-reactive protein, as a result of exhaustive exercise consisting of three intermittent bouts of 800 m at max speed
interspersed with 30-s recovery intervals.
Methods: Ten healthy volunteers were recruited. Anthropometric and V0
data were obtained in the laboratory and venous parameters of basal and immediate post-exercise CK, pH, lactate, complement and C-reactive protein were obtained on an
open-air running track three days later.
Results: Signifi cant increases in plasma CK (114.7±80.3, p=0.005) and lactate (17.27±5.5, p=0.005) were noted. Both parame-
ters, increased CK and lactate post-exercise, correlated signifi cantly (r=0.751, r2=0.574, p=0.012). The complement system
Key words:
was activated, with the increase in CK predicting the increase in C3 (p=0.003). No post-exercise increase in C-reactive protein Conclusion
: The systemic infl ammatory response measured in terms of increases of the complement C3 and 4 was activated by exhaustive exercise. New studies are required to determine the physiological benefi t of this activation, and discriminate it from the prejudicial eff ects this activation could cause in other settings.
Efecto del ejercicio intenso en el Sistema Inmune, medido a través de la activación del Complemento y de la Proteína C-reactiva La infl uencia del ejercicio en la respuesta infl amatoria sistémica ha sido objeto de debate desde hace más de diez años, sin
embargo son muy escasos los estudios originales que hayan analizado su activación y son practicamente inexistentes los
estudios translacionales que hayan extrapolado los resultados analíticos a la realidad de los deportistas.
Objetivo: El objetivo de este trabajo ha sido determinar el efecto del ejercicio intenso sobre dos marcadores infl amatorios
conocidos: la activación del Complemento y de la Proteína C-reactiva.
Métodos: Diez deportistas sanos y bien entrenados fueron sometidos, después de fi rmar el consentimiento informado,
a tres series consecutivas de 800 metros a velocidad máxima con intervalos de 60 segundos entre series en pista abierta.
Inmediatamente antes y después del ejercicio se tomaron muestras de sangre venosa para determinación de CK, pH,
Lactato, Complemento y Proteína C-reactiva. Tres días antes, en el Laboratorio de Medicina Deportiva se realizó un estudio
Antropométrico y cálculo de V0
Resultados: Se obtuvieron incrementos signifi cativos en CK plasmática (114,7 ± 80,3, p = 0,005) y en lactato (17,27 ± 5,5,
p = 0.005) tras la realización de la prueba en pista. Ambos parámetros, el aumento de CK y lactato después del ejercicio, se
Palabras clave:
correlacionaron signifi cativamente (r = 0,751, r2 = 0,574, p = 0,012). El incremento de CK actuó como factor predictor de la elevación de la fracción C3 del Complemento (p = 0,003). La Proteína C-reactiva no se incrementó tras el ejercicio. Conclusión: El ejercicio intenso funcionó como factor de activación inmediato de la respuesta infl amatoria sistémica medida
en términos de elevación de las fracciones C3 y 4 del complemento. Se requieren nuevos estudios para determinar el bene- fi cio fi siológico de esta activación y discriminar los efectos perjudiciales que esta activación podría causar en otros entornos.
Correspondencia: Ana Navarro-Sanz
E-mail: miradordealbion@hotmail.com
Arch Med Deporte 2013;30(6):260-270
Effect of exhaustive exercise on the immune system, measured through complement activation and C-reactive protein The study comprised two phases. The fi rst phase took place in the The immune system is a complex network distributed throughout laboratory and the second phase took place 72 hours later on an open- the body and composed of several cell lines and over a hundred water- air running track. All the subjects already had previous experience with soluble molecules, all intrinsically linked1, whose initial function is the treadmill exercises. At the laboratory visit, an anthropometric study was restoration of homeostatic conditions and the elimination of agents made at rest and measurements were taken of blood pressure, heart that could alter homeostasis2. Despite this healing role, changes in its rate and maximal cardiopulmonary exercise during a treadmill test. own self-control mechanisms have led to situations of aggression to This test was performed on a motorized treadmill (PowerJog Version 5, the organism itself, as in certain autoimmune diseases3,4 or in critically Serie J Mod J200. Birminghan, UK). During the test a complete 12-lead ill patients in situations of multiple organ failure5, where an exaggerated ECG monitoring was done (Norav Medical Ltd 1200s v 5.0.1 Wiesbaden, response or a response maintained over time may lead to metabolic Germany). The ambient temperature during the study ranged from 19 autophagy disorders or indiscriminate harm to the body's own tissues.
to 20ºC and the relative humidity from 55-60%. For the 24 h prior to Currently various associations are known between exercise and the the study the participant was required to abstain from physical exercise immune response6. Strenuous exercise could cause activation of the and the consumption of alcohol, caff eine and soft drinks. The maximum immune response by cellular destruction of ischemic or traumatic origin, the purpose of which is to restore homeostasis through the recovery of termined using a ramp protocol. The treadmill inclination was set at 3% injured cells and cell removal from irreversibly injured tissues7. This me- throughout the test. A three-minute warm-up period was performed at 4 chanism may activate the immune system, via the classic complement km h-1 and the initial test workload was 6 km h-1. The speed was increased (C) pathway and other acute phase proteins involved in the immune 2 km h-1 every two minutes until exhaustion. The tests were considered response, such as C-reactive protein (CRP). As there is involvement of as maximal if the subjects satisfi ed at least one of the following two heterogeneous cell lines, with diverse molecules with a diff erent half- criteria: (a) maximum voluntary exhaustion defi ned by attaining a 10 life and an irregular distribution, various diff erent measurements have on the Borg CR-10 scale; (b) 90% of the predicted HR been used to measure the infl ammatory response to exercise. However, a heart rate plateau between two consecutive work rates. The absolute the various studies involve diff erent exercise patterns and very diverse values were obtained by applying the ACSM equation13: 3.5 (ml and heterogeneous populations, all of which hinder comparison of kg-1 min-1) + 0.2 (speed m min-1) + 0.9 (speed m min-1) x 0.03 the analytical results obtained in the various clinical trials of immune At the open-air running track 72 hours after the laboratory study activation secondary to strenuous exercise8-10.
the participants ran three bouts of 800 meters at maximum velocity, We report a study involving a group of elite, middle distance interspersed with 30-s recovery intervals. Previously they had performed runners who ran three consecutive 800-meter series on an outdoor a 20-minute warming period. Twenty ml of venous blood were drawn track at full speed, after which we analyzed muscle damage infl icted from an antecubital vein at baseline and immediately after fi nishing the by Creatine kinase (CK) elevation and the immune response against last bouts. Whole venous blood was collected in serum-gel vacutainer this damage by determining the activation of the complement system tubes and allowed to clot for ~30 min. After centrifugation at 4000 rpm, one sample of serum was aliquoted, frozen and stored at −80°C for later analysis, and another sample was immediately analyzed for creatin kinase (CK), C-reactive protein (CRP), and C3 and C4. Two fi nal samples, taken at baseline and after the test, were used for blood gases and lactate measurement in venous blood with 80 IU electrolyte-balanced heparin The CK concentration was measured by an enzymatic reaction. C3, Ten healthy sports volunteers were selected for the study (5 men, C4 and CRP were measured by immunonephelometry (Dimension Vista, 5 women). All were elite middle distance runners. Their mean age was Siemens Healthcare, Diagnostic Products GmbH Marburg, Germany). The 28.7 (4.7) years, the body mass index (BMI) was 20.87 (2.27) kg/m2, the pH and pCO were measured by potentiometry with selective electro- muscle percentage was estimated at 44.76 (3.39), and the fat percen- des and the pO and lactate by amperometry with selective electrodes tage at 13.85 (3.67). The muscle and fat percentages were estimated (both techniques from ABL Flex Radiometer, Copenhagen, Denmark). using the Statement of the Spanish Group of Kinanthropometry of the The results are expressed as –log [H+] (normal range 7.36-7.46), lactate Spanish Federation of Sports Medicine11 and ISAK (International Society as mM/L (normal range <2), CK as U/L (normal range <300), C3/C4 as for the Advancement of Kinanthropometry)12. All the subjects had been mg/dL (normal range 60-140 and 10-40, respectively) and PCR as mg/L involved in aerobic activities for at least three years, six times per week, 120-150 minutes per day. At the time of the study the subjects were at the end of the training season. All the participants were informed of the potential risks and discomfort associated with the exercise testing protocols and blood drawing, and subsequently provided written The numerical values were analyzed calculating the mean ± stan- dard deviation (SD). Comparison of related means (SD) was done with Arch Med Deporte 2013;30(6): 260-270
the Wilcoxon non-parametric test. The correlation between variables exercise. CK and pH variations showed signifi cant variations before and was determined using the Pearson linear correlation test, obtaining the after the intermittent exercise bouts (pH = 0.005). Lactate showed an nation. The Pearson and Wilcoxon tests were considered signifi cant if Table 3 shows the individual and mean (SD) results of C3, C4 and the p<0.05. To study the relation of causality a multiple linear regression CRP before and after the intermittent exercise bouts. C3 and C4 were model was used, including the increase in C3 as the dependent variable signifi cantly elevated after the intermittent exercise bouts (p=0.005 and and the percentage increase in CK, the reduction in pH and the post- p=0.014 respectively). CRP showed no increase.
exercise lactate value as independent variables. The statisitcal analyses There is a correlation between CK percentage increase vs. lactate results after exercise, with a Pearson correlation coeffi cient of determination (r2) of 0.574 (p=0.012) Figure 1 shows the correlation between CK percentage increase vs lactate results after the exercise, giving a Pearson correlation coeffi Table 1 shows the epidemiologic results concerning age and sex cient of determination (r2) of 0.574 (p=0.012) distribution, expressed as individual and mean (SD), as well as the anthro- Figure 2 shows the correlation between CK percentage increase pometric results relating to BMI, muscle and fat percentage expressed vs C3 increase, giving a Pearson correlation coeffi as individual and mean (SD), as well as V0 cient of determination (r2) of 0.717 (p=0.002). min-1 as individual and mean (SD), and fi nally the individual and mean Similar results were found after correlating the post-exercise lactate (SD) increase in heart rate and systolic blood pressure at resting and after the treadmill test. These data were all obtained in the laboratory.
No signifi cant results were found with C4 variation vs CK percentage Table 2 shows the individual and mean (SD) results of CK and pH increase or post-exercise lactate, though there was a trend towards a before and after the intermittent exercise bouts and lactate after the Table 1. Epidemiological, anthropometric and clinical fi ndings.
Mean (SD)
28.7 (4.7)
20.87 (2.2)
13.8 (3.6)
44.76 (3.4)
59.8 (4.7)
112 (4.1)
BMI: Body Mass Index; %: muscle percentage; V0 : maximum oxygen consumption;HR: increased heart rate; SBP: increased systolic blood pressure.
Table 2. Absolute values and variations in CK, pH and lactate levels before and after the three exercise bouts, expressed as mean (SD).
CK-pre (*)
CK-post (*)
pH-pre (*)
pH-post (*)
pH Lact-post
Mean (SD)
254.5 (189.8)
369.2 (260.9)
114.7 (80.3)
7.37 (0.02)
7.10 (0.03)
0.27 (0.09)
17.27 (5.5)
Arch Med Deporte 2013;30(6): 260-270
Effect of exhaustive exercise on the immune system, measured through complement activation and C-reactive protein Table 3. C3, C4 and CRP before and after the test, plus the increase from the fi rst to the second measurement, expressed as mean ±
standard deviation.

Case C3-pre(*)
C3-post(*)
C3 C4-pre(*) C4-post(*)
PCR- post
Mean (SP)
87,70 (±8,52) 124,5 (±28,16) 36,8 (±26,41)
19,8 (±5.84)
25,44 (±11,9)
5,77 (±6,41)
C3-pre: C3 before the test; C3-post: C3 after the test; C3: increase in C3; C4-pre: C4 before the test; C4-post: C4 after the test; C4: increase in C4; PCR-pre: PCR before the test; CRP-post: CRP after the test; *signifi cant pre-post diff erence (p<0.05).
Figure 1. Correlation coeffi
cient between the percentage increase
Figure 2. Correlation coeffi
cient between the percentage increase
in CK and the post-exercise lactate values. There was a signifi cant
in CK and the variation in C3 after the exercise. There was a sig-
correlation between the two variables, with a Pearson correlation
nifi cant correlation between the two variables, r = 0.847 and r2 =
cient = 0.75 and a determination coeffi
cient = 0.574 (p =
0.717, (p = 0.002).
The multiple linear regression model showed that the percentage do not necessarily have a clinical impact in healthy athletes with a increase in CK predicted the percentage increase in C3 (p = 0.003). No normal baseline immune system. Traditionally, the diff erence has been attributed to whether the exercise is performed in exhaustive conditions or aerobic conditions for a non-competitive purpose, which have very diff erent metabolic and hormonal environments. Our study population comprised healthy, young, well-trained runners in an excellent physical The eff ect of strenuous exercise on the immune system has been condition, as can be seen from the anthropometric and maximal oxygen of great interest for over a decade. An activating as well as a depressing consumption reported in Table 1. The runners exercised strenuously, eff ect of the immune response has been attributed to exercise activity, evidenced by the remarkable change in blood pH (resulting from the without clarifying which is predominant14. Extrapolating the experi- increased lactic acid) and the post-exercise elevation in CK (see Table mental fi ndings to clinical experience is even more diffi 2). Other authors have tried to correlate decreases in pH with the abi- signifi cant changes in the immune response found in the laboratory lity to recover, using this decrease as an important indicator to avoid Arch Med Deporte 2013;30(6): 260-270
overtraining or excessive exercise-induced muscle damage, leading been implicated in many proinfl ammatory functions, especially at the to a lower athletic performance in subsequent sessions15. However, as beginning of the chain of recognition of aggressions28 and activation pH measurement is an invasive procedure requiring drawing of blood of the complement system and other proinfl ammatory cytokines29. It immediately after the exhaustive exercise, noninvasive determinations, is striking that no increase was detected in our population, suggesting such as near-infrared refl ectance spectroscopy, have been sought, with that our model of aggression does not activate CRP production or some authors fi nding good correlations16. Nevertheless, we believe that that its elevation takes place later. Other authors have measured its these new tests require further validation since their methodology is concentration several hours after the conclusion of vigorous exercise cult to perform on an outdoor track and and found it signifi canty elevated30 or slightly elevated31. In our series in the laboratory. Some authors have studied the behavior of the pH the rise in the complement system without an increase in CRP suggests within the exercise-induced damaged muscle, in which even more independent CRP pathways of complement activation.
severe decreases in pH have been observed than those found by us in The C system is a complex network of about 30 substances, most venous blood17. However, comparisons cannot be made between the of them soluble and some membrane-bound macrophages32, whose two measurments (intracellular and extracellular) as it has long been function is the recognition of foreign substances, opsonization of the known that intracellular pH levels are lower than extracellular pH levels, macrophage-lymphocyte system and the destruction of invading microorganisms or the damaged cells themselves. Three activation Other authors have observed changes in the plasma concentration pathways are recognized: (a) the classical pathway, activated by immu- of CK after strenuous exercise19-21, results that are consistent with ours. nocomplexes, (b) the alternative pathway, which does not require the In our study, the increase in CK would have been more marked if serial formation of immunecomplexes and can be activated by viruses, cell measurements had been made during the fi rst 24 hours, given the fractions, or other acute phase proteins, and (c) the pathway initiated kinetics of CK in the presence of muscular damage of any origin22. In by the mannose-binding lectin33. The C3 and C4 fractions of the comple- some extreme cases, the CK increase has resulted in rhabdomyolysis ment system act as opsonizing and activating agents of the cellular and complicated by acute renal failure23. Anyway, the increase in CK in molecular pathway of infl ammation. We chose to study the C3 and C4 cient to show muscle damage secondary to fractions because they are readily measurable in the clinical laboratory, exercise. The correlation found between the percent increase in CK and they are part of the immune response activated by attacks of various degree of metabolic acidosis, measured in terms of pH and lactic acid, kinds, not just microbial, and because they are the acute-phase proteins suggests that the muscular damage may result from the hypoxia and anaerobic metabolism to which the muscle is exposed, and not just All our patients had normal baseline C3 and C4 values. An increase from the local traumatic damage resulting from stroke. However, we >25%, which is the minimum increase to be considered as an acute- have found no publications examining the relations between CK and phase protein34, was observed after the three intermittent bouts. C pH comparing types of exercises with (running) and without (cycling) activation after exercise has been considered an inductor of the chro- direct muscle trauma. Our results showed a signifi cant correlation bet- nic fatigue syndrome35, though it has been found to be increased in ween the percent increase in CK and post-exercise lactate, though it is healthy youngs males after prolonged exercise36. Our results suggest not possible to determine whether the CK increase was secondary to the C system is one of the activation pathways of immunity, aimed at lactic acidosis or to the exercise-induced trauma.
restoring homeostasis after strenuous exercise. However, further studies The infl ammatory response is made up of a dense network of are needed to understand the chronological evolution of C activation substances, mostly hepatic synthetic polypeptides1, with multiple mo- and its defi nitive role in repairing damaged tissues.
dulating and overlapping functions. It is to notable that such diff erent A correlation was observed between the elevations of CK and C3, processes as are strenuous exercise or a serious systemic infection suggesting that the intensity of the C system activation is correlated both activate the same mediators, with sometimes paradoxical results. with the intensity of muscle damage, as measured in terms of CK eleva- Thus, a prolonged infl ammatory response over time can cause tissue tion. Furthermore, the multiple regression model showed a signifi cant damage that magnifi es and perpetuates the infl ammatory response correlation, indicating that the increase in CK is causing the activation and may fi nally lead to the systemic infl ammatory response syndrome of C3. The relation between CK and C4, however, was not signifi cant, (SIRS), multiple organ failure (MOF) and even death of the individual24 though the trend was similar. We believe that inclusion of more cases whereas the body's infl ammatory response should restore normal would have resulted in a signifi cant association.
conditions. Understanding the intensity of the response and its evolu- A limitation of our study is that the measurements were not repea- tion over time could be helpful in directing the body's infl ammatory ted at diff erent times. This would have helped to know the chronological response to various insults25, and such knowledge could lead to lines intensity of the activation, but this would require serial extraction of of treatment of certain diseases caused by external aggression, as well blood. It should be noted, though, that the participants undertook as to better comprehension of the role of the diff erent components of strenuous exercise every day, so the baseline values reported were also the values found within 24 hours of completing the exercise of The CRP levels before and after the test were <2.9 mg/L, compatible the day before, by which time they had returned to normal, suggesting with the normal reference values in our laboratory. CRP was fi rst isolated the response is transient. What we do have, however, is a refl ection of in 1930, in response to pneumococcal polysaccharide C27, and it has the activated immune system immediataly after exhaustive exercise.
Arch Med Deporte 2013;30(6): 260-270
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