Int J Sports Med 2018; 39(14): 1041-1048
DOI: 10.1055/a-0723-4421
Physiology & Biochemistry
© Georg Thieme Verlag KG Stuttgart · New York

Circulating Inflammatory Cytokine Responses to Endurance Exercise in Female Rowers

Jaak Jürimäe
1   Institute of Sport Sciences and Physiotherapy, University of Tartu,Tartu, Estonia
,
Sille Vaiksaar
1   Institute of Sport Sciences and Physiotherapy, University of Tartu,Tartu, Estonia
,
Priit Purge
1   Institute of Sport Sciences and Physiotherapy, University of Tartu,Tartu, Estonia
› Author Affiliations
Further Information

Publication History



accepted 20 August 2018

Publication Date:
12 November 2018 (online)

Abstract

This investigation examined the effects of acute rowing exercise on a panel of 12 different inflammatory cytokines. Fifteen female rowers (18.3±1.6 yrs; 172.0±5.0 cm; 67.5±8.8 kg; maximal oxygen consumption [VO2max]: 47.2±7.9 ml.min.−1kg−1) completed a 1-h endurance exercise (distance: 12.1±1.1 km; energy expenditure [EE]: 639±69 kcal; heart rate: 151±7 beats.min−1; intensity: 79.6±3.5% of the second ventilatory turn point). Venous blood samples were analysed for interleukin (IL)-2, IL-4, IL-6, IL-8, IL-10, vascular endothelial growth factor (VEGF), interferon-gamma (IFN-γ), tumor necrosis factor-alpha (TNF-α), IL-1α, IL-1β, monocyte chemoattractant protein-1 (MCP-1) and epidermal growth factor (EGF) concentrations. Rowing exercise resulted increment (P<0.05) in IL-6, IL-8, VEGF and MCP-1. Exercise metabolic demand variables such as rating of perceived exertion (r=0.61), distance covered (r=0.60) and EE (r=0.57) were related (P<0.05) to changes in VEGF concentration. Cardiorespiratory fitness as measured by VO2max was correlated with changes in IL-6 (r=–0.55; P<0.05) level. In conclusion, acute exercise-induced inflammatory reaction was induced by a significant increase in IL-6, IL-8, VEGF and MCP-1 concentrations. Variance in exercise-induced increases in inflammatory cytokines in response to prolonged endurance exercise was characterised by exercise metabolic demand and cardiorespiratory fitness measures in female rowers.

 
  • References

  • 1 Accattato F, Greco M, Pullano SA, Care I, Fiorillo AS, Pujia A, Montalcini T, Foti DP, Brunetti A, Gulletta E. Effects of acute physical exercise on oxidative stress and inflammatory status in young, sedentary obese subjects. Plos One 2017; 12: e0178900
  • 2 Beavers KM, Brinkley TE, Nicklas BJ. Effect of exercise training on chronic inflammation. Clin Chim Acta 2010; 41: 785-793
  • 3 Borg G. Perceived exertion as indicator of somatic stress. Scand J Rehabil Med 1970; 2: 92-98
  • 4 Casazza GA, Jacobs KA, Suh SH, Miller BF, Horning MA, Brooks GA. Menstrual cycle phase and oral contraceptive effects on tryglyceride mobilization during exercise. J Appl Physiol 2004; 97: 302-309
  • 5 Church TS, Barlow CE, Earnest CP, Kampert JB, Priest EL, Blair SN. Associations between cardiorespiratory fitness and C-reactive protein in men. Arterioscler Thromb Vasc Biol 2002; 22: 1869-1876
  • 6 Comassi M, Vitolo E, Pratali L, Del Turco S, Dellanoce C, Rossi C, Santini E, Solini A. Acute effects of different degrees of ultra-endurance exercise on systemic inflammatory responses. Intern Med J 2015; 45: 74-79
  • 7 Dean TM, Perrault L, Mazzeo RS, Horton TJ. No effect of menstrual cycle phase on lactate threshold. J Appl Physiol 2003; 95: 2537-2543
  • 8 Delavar H, Nogueira L, Wagner PD, Hogan MC, Metzger D, Breen MC. Skeletal myofiber VEGF is essential for the exercise training response in adult mice. Am J Physiol Regul Integr Comp Physiol 2014; 306: R586-R595
  • 9 Dill DB, Costill DL. Calculation of percentage changes in volumes of blood, plasma and red cells in dehydration. J Appl Physiol 1974; 37: 247-248
  • 10 Fatouros I, Chatzinikolaou A, Paltoglou G, Petridou A, Avloniti A, Jamurtas A, Goussetis E, Mitrakou A, Mougios V, Lazaropoulou C, Margeli A, Papassotiriou I, Mastorakos G. Acute resistance exercise results in catecholaminergic rather than hypothalamic-pituitary-adrenal axis stimulation during exercise in young men. Stress 2010; 13: 461-468
  • 11 Frayn KN. Calculation of substrate oxidation rates in vivo from gaseous exchange. J Appl Physiol 1983; 55: 628-634
  • 12 Green AN, McGrath R, Martinez V, Taylor K, Paul DR, Vella CA. Associations of objectively measured sedentary behavior, light activity, and markers of cardiometabolic health in young women. Eur J Appl Physiol 2014; 114: 907-919
  • 13 Gustafson B. Adipose tissue, inflammation and atherosclerosis. J Atheroscler Thromb 2010; 17: 332-341
  • 14 Harriss DJ, Macsween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 update. Int J Sports Med 2017; 38: 1126-1131
  • 15 Henson DA, Nieman DC, Nehlsen-Cannarella SL, Fagoaga OR, Shannon M, Bolton MR, Davis JM, Gaffney CT, Kelln WJ, Austin MD, Hjertman JME, Schilling BK. Influence of carbohydrate on cytokine and phagocytic responses to 2 h rowing. Med Sci Sports Exerc 2000; 32: 1384-1389
  • 16 Hofmann P, Jürimäe T, Jürimäe J, Purge P, Mäestu J, Wonisch M, Pokan R, von Duvillard SP. HRTP, prolonged ergometer exercise, and single sculling. Int J Sports Med 2007; 28: 964-969
  • 17 Hoier B, Hellsten Y. Exercise-induced capillary growth in human skeletal muscle and the dynamics of VEGF. Microcirculation 2014; 21: 301-314
  • 18 Ives S, Blegen M, Coughlin MA, Redmond J, Matthews T, Paolone V. Salivary estradiol, interleukin-6 production, and the relationship to substrate metabolism during exercise in females. Eur J Appl Physiol 2011; 111: 1649-1658
  • 19 Jürimäe J, Jürimäe T, Purge P. Plasma testosterone and cortisol responses to prolonged sculling in male competitive rowers. J Sports Sci 2001; 19: 893-898
  • 20 Jürimäe J, Hofmann P, Jürimäe T, Palm R, Mäestu J, Purge P, Sudi K, Rom K, von Duvillard SP. Plasma ghrelin responses to acute sculling exercises in elite male rowers. Eur J Appl Physiol 2007; 99: 467-474
  • 21 Jürimäe J, Mäestu J, Jürimäe T, Mangus B, von Duvillard SP. Peripheral signals of energy homeostasis as possible markers of training stress in athletes: a review. Metab Clin Exp 2011; 60: 335-350
  • 22 Jürimäe J, Tillmann V, Purge P, Jürimäe T. Acute inflammatory response to prolonged sculling in competitive male rowers. J Sports Med Phys Fitness 2016; 56: 1368-1375
  • 23 Jürimäe J, Tillmann V, Purge P, Jürimäe T. Body composition, maximal aerobic performance and inflammatory biomarkers in endurance-trained athletes. Clin Physiol Funct Imaging 2017; 37: 288-292
  • 24 Kullo IJ, Khaleghi M, Hensrud DD. Markers of inflammation are inversely associated with VO2max in asymptomatic men. J Appl Physiol 2007; 102: 1374-1379
  • 25 Landers-Ramos RQ, Jenkins NT, Spangenburg EE, Hagberg JM, Prior SJ. Circulating angiogenic and inflammatory cytokine responses to acute aerobic exercise in trained and sedentary young men. Eur J Appl Physiol 2014; 114: 1377-1384
  • 26 Maeda S, Suguwara J, Yoshizawa M, Otsuki T, Shimojo N, Jesmin S, Ajisaka R, Miyauchi T, Tanaka H. Involvement of endothelin-1 in habitual exercise-induced increase in arterial compliance. Acta Physiol (Oxf) 2009; 196: 223-229
  • 27 Maggio M, Ceeda GP, Lauretani F, Bandinelli S, Corsi AM, Giallauria F, Guralnik JM, Zuliani G, Cattabiani C, Farrino S, Ablondi F, Dalláglio E, Ceresini G, Basaria S, Ferrucci L. SHBG, sex hormones, and inflammatory markers in older women. J Clin Endocrinol Metab 2011; 96: 1053-1059
  • 28 Nieman DC, Henson DA, Smith LL, Utter AC, Vinci DM, Davis JM, Kaminsky DE, Shute M. Cytokine changes after a marathon race. J Appl Physiol 2001; 91: 109-114
  • 29 Nieman DC, Dumke CL, Henson DA, McAnulty SR, Gross SJ, Lind RH. Muscle damage is linked to cytokine changes following a 160-km race. Brain Behav Immun 2005; 19: 398-403
  • 30 Nieman DC, Konrad M, Henson DA, Kennerly K, Shanely RA, Wallner-Liebmann SJ. Variance in the acute inflammatory response to prolonged cycling is linked to exercise intensity. J Interferon Cytokine Res 2012; 32: 12-17
  • 31 Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 2008; 88: 1379-1406
  • 32 Rämson R, Jürimäe J, Jürimäe T, Mäestu J. The influence of increased training volume on cytokines and ghrelin concentration in college level male rowers. Eur J Appl Physiol 2008; 104: 839-846
  • 33 Rhea MR. Determining the magnitude of treatment effects in strength training research through the use of the effect size. J Strength Cond Res 2004; 18: 918-920
  • 34 Sciberras JN, Galloway SDR, Fenech A, Grech G, Farrugia C, Duca D, Mifsud J. The effect of turmeric (curcumin) supplementation on cytokine and inflammatory marker responses following 2 hours of endurance cycling. J Int Soc Sports Nutr 2015; 12: 5
  • 35 Shanely RA, Nieman DC, Henson DA, Jin F, Knab AM, Sha W. Inflammation and oxidative stress are lower in physically fit and active adults. Scand J Med Sci Sports 2013; 23: 215-223
  • 36 Skaparpanska-Stejnborn A, Basta P, Trzeciak J, Szczesniak-Pilaczynska L. Effect of intense physical exercise on hepcidin levels and selected parameters of iron metabolism in rowing athletes. Eur J Appl Physiol 2015; 115: 345-351
  • 37 Smith LL. Cytokine hypothesis of overtraining: a physiological adaptation to excessive stress?. Med Sci Sports Exerc 2000; 32: 317-331
  • 38 Steinacker JM, Lormes W, Reissnecker S, Liu Y. New aspects of the hormone and cytokine response to training. Eur J Appl Physiol 2004; 91: 382-391
  • 39 Suh SH, Casazza GA, Horning MA, Miller BF, Brooks GA. Luteal and follicular glucose fluxes during rest and exercise in 3-h postabsorptive women. J Appl Physiol 2002; 93: 42-50
  • 40 Sureda A, Mestre-Alfaro A, Banquells M, Riera J, Drobnic F, Camps J, Joven J, Tur JA, Pons A. Exercise in a hot environment influences plasma anti-inflammatory and antioxidant status in well-trained athletes. J Therm Biol 2015; 47: 91-98
  • 41 Suzuki K, Totsuka M, Nakaji S, Yamada M, Kudoh S, Liu Q, Sugawara K, Yamaya K, Sato K. Endurance exercise causes interaction among stress, hormones, cytokines, neutrophil dynamics, and muscle damage. J Appl Physiol 1999; 87: 1360-1367
  • 42 Suzuki K, Yamada M, Kurakake S, Okamura N, Yamaya K, Liu Q, Kudoh S, Kowatari K, Nakaji S, Sugawara K. Circulating cytokines and hormones with immunosuppressive but neutrofil-priming potentials rise after endurance exercise in humans. Eur J Appl Physiol 2000; 81: 281-287
  • 43 Utsal L, Tillmann V, Zilmer M, Mäestu J, Purge P, Jürimäe J, Saar M, Lätt E, Maasalu K, Jürimäe T. Elevated serum IL-6, IL-8, MCP-1, CRP, and IFN-γ levels in 10- to 11-year-old boys with increased BMI. Horm Res Paediatr 2012; 78: 31-39
  • 44 Vaiksaar S, Jürimäe J, Mäestu J, Purge P, Kalytka S, Shakhlina L, Jürimäe T. No effect of menstrual cycle phase on fuel oxidation during exercise in rowers. Eur J Appl Physiol 2011; 111: 1027-1034
  • 45 Venables MC, Achten J, Jeukendrup AE. Determinants of fat oxidation during exercise in healthy men and women: a cross-sectional study. J Appl Physiol 2005; 98: 160-167
  • 46 Yardley M, Ueland T, Aukrust T, Michelsen A, Bjorkelund E, Gullestad L, Nytroen K. Immediate response in markers of inflammation and angiogenesis during exercise: a randomized cross-over study in heart transplant recipients. Open Heart 2017; 28: e000635