Tartibian B. et al.
EQOL (2009) 49-55
THE EFFECTS OF 8 WK INTENSIVE JUDO TRAINING
ON THE HUMORAL IMMUNE SYSTEM IN JUDO
FIGHTERS
Bakhtyar Tartibian*, Asghar Abbasi**, and Hirash Nouri*
* Department of Physical Education and sport science., Urmia University, Urmia., Iran
** Institute of Clinical and Experimental Transfusion Medicine
(IKET), University of Tuebingen,
Otfried-Mueller Tuebingen, Germany
Abstract
The influence of intensive Judo training on serum immunoglobulins IgG, IgM, and IgA was studied in 24
Judo fighters. Subjects were assigned to an exercise training group (EXE; n=12) and non-exercise control
group (Con; n=12). Subjects in EXE group participated in exercise sessions 4 days a week for 8 wk.
Serum samples were collected before, immediately and 1wk after study period. The IgG levels were
significantly increased immediately after exercise training (p=0.001) in EXE compared to Con. However,
IgM and IgA concentrations showed significant decrease immediately after exercise in EXE (p=0.001).
The concentrations of all immunoglobulins had returned to baseline by 1wk of recovery. In conclusion
the increased IgG levels are possibly due to isotype switching or a secondary antibody responses that
could be considered as enhancement in immune system function. However, chronic suppression of
immuniglobulins IgM and IgA may be mediated by hormonal changes associated with exhausting
exercise.
Keywords: Exercise immunity; Judo Fighters; Serum Immunoglobulins
Introduction
Despite the numerous studies aimed at explaining the specefic immune system responses to exercise,
there is no agreement in the results obtained so far from these studies. Most of the studies examining the
effects of the exercise on immune function, have either focused on only one bout of exercise or the
changes following exercise of short duration (1,5). There are limited studies investigating the effect of
regular exercise at long term on the immune system (1,10,41). Regular exercise with moderate impact is
known to strengthen the immune system and increase the resistance against stress (6,11,14,22,27,21). On
the other hand it is also known that vigrous exercise can have negaive effects on these functions
(5,24,40,42). Data on serum immunoglobulin levels in athlets are controversial. Several studies have
shown clinicaley normal serum Ig concentration in athlets
(1,4,35). Some have shown increases
(31,34,37) and some have shown lower Ig levels in athletes compared with control subjects (23,28,37,6).
However, few studies have investigated the effects of extensive exercise training on serum
immunoglobulin (Ig) status. Serum Ig concentrations showed little or no change after acute exercise in
trained runners, especially when Ig concentrations are corrected for changes in plasma volume (10).
Stephensen et al (12) and Poortmans (39) have reported significant increases in immunoglobulins A and
G levels and no change in IgM levels following maximal exetcises. However, a significant decrease in
IgG and IgM Levels after 3 month training (130 to 140 min, 5-7 days per week) and a significant increase
in IgG and IgA concentrations after 15 min intensive exercise were reported by Garagiola (13) and Wit
(49) respectively. Verder (47) showed reduction of IgA and IgM concentrations of elite athlets following
short term acute exercise. However, an increase in serum antibody concentrations due to maximal and
submaximal exercise have been reported by Nieman (32,34,35,45). Despite numerous studies, no studies
are available concerning the effects of Judo specific training on immunoglobulin levels. The influence of
acute and long term exercise period on the immunoglobulin responses is important for the trainers and
coaches who work and design training programs for amateur and proffesional athlets especially Judo
49
Tartibian B. et al.
EQOL (2009) 49-55
players. For this reason, our study was aimed to investigate the effects of long term Judo specefic training
on immunoglobulin levels of Judo fighters.
Methods and Materials
Subjects
24 elite male Judo fighters (mean age 21) who had regular Judo training for an average of 8-10 hr per week,
for at least 5 years, and had fought competitively, were recruited for this study. They were randomized into
two groups: exercise and control groups. The athletes were informed about the exercise training program
and potentional benefits of the study before they signed an informed consent form. The Exe group
participated in an specific exercise program for a period of 8 Wk. The Con group were asked not to
participate in any exercise training program during the study. In addition, all subjects had passed a
complet medical examination before participating exercise program.
Exercise program
Subjects in Exe group conducted an exercise programe involving specific intensive Judo training 4 days a
week for 8 Wk. They were supervised and conducted by experienced instructors. Subjects in the Con
group simply maintained their normal physical activity levels during the study.
Blood sampling
Venous blood samples were collected before, immediately and 1 Wk after (recovery period) the exercise
program. Serum immunoglobulins IgA, IgG, IgM were measured by rate nephelometry using Beckman
Array (Beckman, Brea, CA) analyser.
Statistical analysis
Data were analysed using comercial software (SPSS for windows version 12.0) using General linear
model and dependent t-test.
Results
This study investigated the effects of extensive Judo training on serum immunoglobulins levels of athlets.
The individual characteristics of Judo players are shown in table 1.
IgG. Contrast testing reveald that IgG was significantly elevated immediately after the exercise
program (P=0.001). But at 1 Wk recovery, the IgG concentrations had returned to baseline (table2, Fig1).
IgA. Immediately after the exercise program, there was a significant decrease (P=0.001) in IgA
concentrations. At 1Wk, IgA concentrations had returned to baseline (tables3, Fig1).
IgM. Contrast testing revealed a significant decrease in IgM immediately after exercise program
(P=0.001). However, by 1Wk recovery IgM concentrations had returned to baseline (table4, Fig1).
Table 1. Subjects Characteristics
Age (yr)
Height (cm)
Body Weight Rest HR
Fat%
BMI
(kg)
(beat/min)
(kg/m2)
EXE
21 ± 27.1
33.178 ± 96.3
50.76 ± 72.7
91.57 ± 45.5
78.7 ± 80.1
47.21 ± 70.0
CON
35.21 ± 64.1
75.178 ± 38.3
66.74 ± 84.7
16.57 ± 25.6
40.7 ± 44.1
37.21 ± 57.0
Table 2. Comparison of the mean (and s.d.) of serum IgG levels over the training season from other athletes
and control subjects
Before
Immediately
Recovery
Sig
EXE
64.1008 ± 19.41
54.1123 ± 30.39
65.1024 ± 7.70
*001.0
CON
58.998 ± 79.39
04.1002 ± 76.38
65.1002 ± 72.37
298.0
* p>0/05
50
Tartibian B. et al.
EQOL (2009) 49-55
Table 3. Comparison of the mean (and s.d.) of serum IgA levels over the training season from other athletes
and control subjects
Before
Immediately
Recovery
Sig
EXE
43.238 ± 85.19
57.225 ± 01.20
85.235 ± 72.21
*001.0
CON
96.232 ± 97.22
75.234 ± 24.23
55.235 ± 83.23
412.0
* p>0/05
Table 4. Comparison of the mean (and s.d.) of serum IgM levels over the training season from other athletes
and control subjects
Before
Immediately
Recovery
Sig
EXE
87.182 ± 94.14
79.167 ± 64.14
94.179 ± 60.13
*001.0
CON
85.176 ± 05.10
13.179 ± 35.11
08.180 ± 75.10
311.0
* p>0/05
Fig. 1. Serum IgA, IgG, IgM levels (mean ± SD) for samples collected from athletes and controls over the
training seasons.
Discussion
The focus of many studies has been to identify changes in serum immunoglobulin concentrations after an
acute bout of strenous exercise. However, in this study the discussion will attempt to elucidate changes in
immunoglobulin concentrations after a period of exercise training, Judo training.
An interesting finding in this study was the significant increase in total serum IgG immediately
after the exercise training program. This increase was accompanied by a signigicant decrease in both IgM
and IgA. However, the concentrations of all immunoglobulins had returned to baseline by 1wk recovery.
Generally, in exercise immunology an increase in immunoglobulin concentration has been interpreted to
represent enhanced immunity, and a decrease has usually been interpreted as immunosuppression.
51
Tartibian B. et al.
EQOL (2009) 49-55
McKune et al (30) suggest that alterations in different immunoglobulins may reflect isotype switching
and interaction with innate immune system. With regard to changes in IgG, it appears that research is
conflicting, with few studies measuring this isotype after a period of itensive exercise training. Recently
Petibois et al (37) monitored immunoglobulin alterations over 12 month of rowing training, and like the
present study, found that the IgG increased as the result of exercise. Similarly, Tartibian and Moazeni
(45) reported a significant increase in IgG for Wrestlers in competition phase. But in contrast to our
findings, Mashiko et al (23) found a significant decrease in IgG (-8%) after a 20 day rugby training,
training two hours a day, six days a week. Gleeson M et al (16) also, reported a significant suppressin of
serum IgG in swimmers after long-term intensive swim training. Serum IgG levels decreased with
increasing distances swum by the athlets (16), and the suppression of total IgG levels was reflected
mainly in lower levels of the IgG2 subclass. Alterations induced by shorter acute bouts of exercise and
training have been reported. Poortmans (39) found a significant 12% increase in serum IgG immediately
after a progressive cycle ergometer test to fatigue. However Nieman and Nehlsen (34), found that IgG
decreased during recovery after a three hour run at marathon pace, reaching baseline concentration 21
hours after exercise. McKune et al (30) also reported significant increases (+12%) in IgG immediately
after ultra-endurance exercise. Similar to McKune et al (30) Poortmans and Halambie (38) reported a
significant 7% increase in IgG immediately after a 100 km race. Karacabay et al (20) and Diken et al (8),
also obtained higher values for IgG immediately after 30 minute aerobic exercise and graded exercise to
exhaustion, respectively. However, karacabay et al (21) again, Garagiola (13), Heath (18), Teved et al
(46), reported a significant decrease for IgG immediately after exercise. Israel et al (19) also, reported that
25 hours after a 75 km run at high intensity, IgG was decreased by 22%.
One explanation that has been proposed for the increases in IgG after exercise is that non-
systemic immunoglobulins are flushed out of the secendary lymph storage sites and/or enter the
circulation because of increased lyphatic flow (34). This may have been the reason why IgG returned to
baseline concentrations by recovery after exercise, as they then returned to their storage sites. At present
there is no evidence to support such an assumption (34) Furthermore, if this had been the case, this would
most likely have resulted in significant increases in all immunoglobulins; this did not occur, with certain
immunoglobulins showing significant decreases. The authors of this study like to propose that the
increase in IgG concentration after such intensive training (for example Judo training) suggests antibody
class switching, similar to that which may occur during a secondary antibody response (30). This is a
process that has only recently been described and involves a switch in immunoglobulin isotype from IgM
to IgG (7). This implies that there will be a decrease in measured IgM as it undergoes genetic
rearrangement and is transformed into IgG (7). Isotype switching is coordinated by T helper 2 cytokines
(30) - for example, interleukins 4, 10, and 6- as well as the hypothalamicpituitary-adrenal axis and
sympathetic nervous system
(9). Cortisol
(hypothalamic-pituitary-adrenal axis) and noradrenaline
(norepinephrine) (sympathetic nervous system) have been shown to promote B cell immunoglobulin
isotype switching from IgM to IgG (9). Although the effect of exercise on interleukin 4 has been difficult
to detect, interleukin 10, interleukin 6, cortisol, and noradrenaline have been regularly reported to be
increased by strenuous endurance exercise (25).
In this study, IgM was significantly reduced immediately after the exercise training period and
returned to baseline by 1wk of recovery. To our knowledge no studies have reported concentrations of
IgM after Judo training and only a few reports exist about the intensive exercise training induced
alterations in IgM concentrations. In consistence with our findings, Mashiko et al (23) found that IgM
decreased by 15% after a 20 day rugby training camp, training two hours a day, six days a week. McKune
et al
(30) and Israel et al (19) reported a significant decrease (23% and 10%, respectively) in IgM
concentrations after high intensity running. Gleeson et al (16), also noted a significant decrease of IgM
after long-term intensive swimming training. Karacabay et al (21) found that the IgM concentrations of
athlets, were decreased, but not significantly, after 30 minute aerobic exercise, with returning the baseline
by 5 days recovery. Mackinnon (29) has also shown that moderate exercise but of longer duration has
lead to a significant decrease in plasma IgM levels. Bente et al (2) have shown that moderate exercise of
long duration has led to a suppression of IgM synthesis in cell culturs. But Nieman et al (34,35) reported
that IgM was increased by 7.2% one hour into a three hour run at marathon pace, returning to baseline
concentrations during the recovery period at 21 hours. Petibois et al (37) reported a training induced
increase in IgM concentration in elite rowers over 12 months. Karacabay et al (20) and Diken et al (8)
also showed higher concentrations for IgM immediately and 5 hours after exercise, respectively. It is
possible that the immunoglobulin response depends on the duration of the event. There are some possible
52
Tartibian B. et al.
EQOL (2009) 49-55
explanations for the IgM concentrations detected in our study. Firstly, isotype switching may have
occurred as part of a rapid secondary antibody response. Secondly, the decrease may reflect IgM
interaction with the innate immune system, specifically complement, in response to exercise training
induced tissue damage (34). Immune complexes formed between IgM and complement would have been
rapidly cleared from the circulation (3) reflecting reduced concentrations of IgM in the peripheral blood.
In this study, circulating IgA showed a significant decrease immediately after the exercise
programe, and returned to baseline concentrations by 1wk recovery. It has been suggested that serum IgA
levels are associated with mucosal secretions in the upper respiratory tract (IgA1) and the gastrointestinal
tract (IgA2) (16). Therefore, changes in circulating concentrations were not expected, nor were dramatic
changes noted. But, in agreement with our results, Gleeson et al (16) revealed significant suppression of
serum IgA in athletes after long-term intensive swimming training. Tartibian and Moazeni (45) also found
a significant decrease in serum IgA concentrations for wrestlers during competition phase. They showed
that the concentrations had returned to baseline at recovery period. A significant decrease in IgA
concentrations have been reported by Gleeson et al (15), Wit (49), Mackinnon et al (26), Gregory et al
(17) and Kracabay et al (21). However, Nieman (34), Poortmans (39), Karacabay et al (20) and Diken et
al (8) have shown a significant increase in IgA levels immediately after intensive exercise. The mecanism
of this immunosuppression is unknown, but may be mediated by hormonal changes associated with
exhausting exercise (43). At this study the Judo fighters participated in long-term intensive training.
Therefore one possible explanation for decreasing serum immunoglobulin levels, could be participating in
long-term tarining. Nieman (34) and Garagiola (13) have emphasized on the effect of long-term training
period on the changes (temporarily) of immune system in athletes. It has been suggested that, also, during
prolonged exercise at high intensity, serum cortisol concentrations are significantly elavated above
control levels for severeal hours (33). Cotisol has been related to many of the immunosuppressive
changes experienced immediately and several hours after exercies (36). Because the athletes in this study
undewent hgih intensity training, it is possible that higher work load for a prolonged period and
cocequence hormonal changes are the regulators of serum antibody in Judo fighters.
In conclusion, the results of this study revealed a significant increase in serum IgG levels and a
significant decrease in serum IgM and IgA concentrations immediately after judo training. The increase in
serum IgG levels may represente an enhanced antibody response. Isotype switching or a secondary
antibody responses may regulate this response. The rapid upregulation of such a response probably
afforded protection against pathogen and may help account for the maintenance of wellbeing of Judo
fighters. However, chronic suppression of both immunoglobulins IgM and IgA, may be mediated by
hormonal changes associated with exhausting exercise. The observations provide a framework for
assessment of those athletes who present with fatigue and an apparant infection-prone state. These
athletes may have a reduction of serum and secretion immunoglobulins or levels at the lower end of the
population reference range. Further studies are in place to determine the clinical significance of the
current observations, the mechanisms of immune enhancement and suppression, and implications for
training and management strategies to enhanced immune system function and/or prevent exercise-induced
immune suppression.
Refrences
1. Bauer T, Weisser B. Effect of aerobic endurance exercise on immune function in elderly athletes.
Schweiz Rundsch Med Prax. 2002; 30: 91:153-158.
2. Bente K.P., and D.T. Andres. Br. J. Sports. Med 35:223-230,2001
3. Boes M. Role of natural and immune IgM antibodies in immune responses. Mol Immunol
2000;37:1141-9.
4. Brenner I, Shek PN, Zamecnik J, Shephard RJ. Stress hormones and the immunological responses to
heat and exercise. Int J Sports Med 1998; 19:130-143.
5. Callow KA. Effect of specific humoral immunity and some nonspecific factors on resistance of
volunteers to respiratory coronavirus infection. J Hyg 1985; 95:173-189.
53
Tartibian B. et al.
EQOL (2009) 49-55
6. Cannon JG. Fiatarone M.A, Fieldinig RA, Evans WJ. Aging and stress induced changes in
complement activation and neutrophil mobilization. J Appl Physiol 1994; 76:2616-2620.
7. Coffman RL, Lebman DA, Rothman P. Mechanism and regulation of immunoglobulin isotype
switching. Adv Immunol 1993;54:229-70
8. Diken H., M. Kelle., L. Colpan., C. Tomer., A. Ermet. Effect of physical exercise on complement and
immunoglobulin levels in wrestlers and sedentary controls. DICLE TIP DERGISI (JOURNAL
MEDICAL SCHOOL) 27: 83-4, 2000
9. Elenkov IJ, Wilder RL, Chrousos GP, et al. The sympathetic nerve: an integrative interface between
two supersystems: the brain and the immune system. Pharmacol Rev 2000;52:595-638.
10. Fahlman MM, Engels HJ, Morgan AL, Kolokouri I. Mucosal IgA response to repeated wingate tests
in females. Int J Sports Med 2001; 22:127-131.
11. Ferry, A, F. Picard ., A. Duvallet ., B. Weill ., and M. Rieu I. Changes in blood leucocyte populations
induced by acute maximal and chronic submaximal exercise. Eur J Appl Physiol 59: 435-442, 1990
12. Filaire E, Bonis J, Lac G. Relationships between physiological and psychological stress and salivary
immunoglobulin A among young female gymnasts. Percept Mot Skills 2004; 99:605-617
13. Garagiola, U. immunological patterns during regular intensive training athletes. J Int Med Res 23:85-
95, 1995
14. Gleeson M (2000). Exerc. Immunol. Rev 6:5-42, 2000
15. Gleeson M., et al. Salivary IgA levels and infection risk in swimmers. Med Sci Sports Exer 31:67-73,
1999
16. Gleeson, M., W. A. Mcdonald., A. W. Crippt., D. B. Pyne., R. L. Clancyt., and P. A. Fricker. The
effect on immunity of long-term intensive training in elite swimmers. Clin Exp Immunol 102:210-
216, 1995
17. Gregory, RL., L.E. Gfell., B.A. King., and J.P. Wallace. Effect of exercise on milk immunoglobulin
A. Med Sci Sports Exerc 29: 1596-1601
18. Heath, G. exercise and upper respiratory tract infection. Sports Med 14: 353-365, 1992
19. Israel S, Buhl B, Neumann G. Die konzentration der immunglobuline A, G und M im serum bei
trainierten und untrainierten sowie nach verschiedenen sportlicken ausdauerleistungen. Med Sport
(Berlin) 22:225-31, 1982
20. Karacabey, K., O. Saygin., R. Ozmerdivenli1., E. Zorba., A. Godekmerdan., and V. Bulut. The
effects of exercise on the immune system and stress hormones in sportswomen. Neuroendocrinology
Letters 4(26): 362-365, 2005
21. Karacabey, K., I. Peker., Ö. Saygun., F. Ciloglu., R. Ozmerdivenli., and V. Bulut. Effects of acute
aerobic and anaerobic exercise on humoral immune system factors in elite athletes. Biotechnol. &
Biotechnol Eq. 19 (1): 175-180, 2005
22. Kenny W. (1995) ACSM´s guidelines for exercise testing and prescription. Baltimore, MD: Willams
& Wilkins, 153-176, 269-287
23. Mashiko T, Umeda T, Nakaji S, et al. Effects of exercise on the physical condition of college rugby
players during summer training camp. Br J Sports Med 38:186-90, 2004
24. Mackinnon, LT. Chronic exercise training effects on immune function. Med Sci Sports Exerc 2000;
32:369-S376.
25. Mackinnon LT. Advances in exercise immunology. Torrens Park, South Australia: Human Kinetics,
1999.
26. Mackinnon, LT., et al. Future diretions in exercise and immunoglobulins regulation and integration.
Int J Sports Med, 19: 205-211, 1998
54
Tartibian B. et al.
EQOL (2009) 49-55
27. Mackinnon, LT. Int J Sports Med, 18(1), 62-68, 1997
28. Mackinnon LT, Hooper SL. Mucosal (secretory) immune system responses to exercise of varying
intensity and during overtraining. Int J Sports Med 15:179-83, 1994
29. Mackinnon, LT. 1992. Exercise and immunology. Human Kinetics Books.
30. McKune A J, L L Smith, S J Semple and A A Wadee: Influence of ultra-endurance exercise on
immunoglobulin isotypes and subclasses. Br. J. Sports Med 39;665-670, 2005
31. Nehlsen-Cannarella SL, Nieman DC, Jessen J, et al. The effects of acute moderate exercise on
lymphocyte function and serum immunoglobulin levels. Int J Sports Med 12:391-8, 1991
32. Nieman D.C et al. . Exercise Immunology. Int J Sports Med, 21: 61-68, 2000
33. Nieman DC. Simandle S. Henson DA et al.:Lymphocyte proliferation response to 2.5 hours of
running. 1nl.J. Sports Med. 16: 404-408 1995.
34. Nieman DC, Nehlsen-Cannarella SL. The effects of acute and chronic exercise and immunoglobulins.
Sports Med 1991;11:183-201.
35. Nieman DC, Tan SA, Lee JW, et al. Complement and immunoglobulin levels in athletes and
sedentary controls. Int J Sports Med 1989;10:124-8.
36. Peter A. Thomas FL et al.: Plasma adrenocorticotropin and cortisol responses to submaximal and
exhaustive exercise. J. Appl. Physiol. Respirat. Environ. Exercise Physiol. 55(5) 1441-1444 1983.
37. Petibois C, Cazorla G, Deleris G. The biological and metabolic adaptations to 12 months training in
elite rowers. Int J Sports Med 2003;24:36-42.
38. Poortmans JR, Haralambie G. Biochemical changes in a 100 km run: proteins in serum and urine. Eur
J Physiol 1979;40:245-54.
39. Poortmans, JR. Serum protein determination during short exhaustive physical activity. J Appli
Physiol 30: 190-190, 1971
40. Reid MR, Drummond PD, Mackinnon LT. The effect of moderate aerobic exercise and relaxation on
secretory immunoglobulin A. Int J Sports Med 2001; 22: 132-137.
41. Sage D, Maurel D, Bosler O. Involvement of the suprachiasmatic nucleus in diurnal ACTH and
corticosterone responsiveness to stress. Am J Physiol Endocrinol Metab 2001; 280:260-269.
42. Simonson SR. The immune response to resistance exercise. J Strength Cond Res 2001; 15:378-384.
43. Smith JA, Weidemann MJ. The exercise and immunity paradox: a neuro-endocrine/cytokine
hypothesis. Med Sci Res 1990; 18:749-53.
44. Stavnezer J. Immunlglobulin class switching. Curr Opin Immunol 1996;8:199-205.
45. Tartibian B and Moezeni. The effects of wrestling training at pre competition and competition phases
on humoral immune system of young wrestlers. Olympic (Iranian Scientific Journal), 10(3,4): 105-
114. 2003
46. Teved, N., et al. evedence that effect of bicycle exercise on blood mononuclear cell proliferation
responses and subset is mediated by epinephrine. Int J Sports Med 15: 100-4, 1994
47. Verder TJ. Eur J Appl Physiol 75: 47-53, 1997
48. Whitham M, Blannin AK. The effect of exercise training on the kinetics of the antibody response to
influenza vaccination. J Sports Sci 21:991-1000, 2003
49. Wit B. Immunological responses of regularly trained athletes. Bio Sports 1: 221-35, 1996
55