Changes in Inflammatory Cytokines and Irisin in Response to High Intensity Swimming in Adolescent versus Adult Male Swimmers

Malcolm Sanderson, Brandon J McKinlay, Alexandros Theocharidis, Rozalia Kouvelioti, Bareket Falk, Panagiota Klentrou, Malcolm Sanderson, Brandon J McKinlay, Alexandros Theocharidis, Rozalia Kouvelioti, Bareket Falk, Panagiota Klentrou

Abstract

Swimming is a popular youth sport that is considered beneficial for cardiovascular fitness. However, the potential inflammatory outcomes of high intensity swimming in younger swimmers are unclear, as is the response of irisin, a myokine released during exercise with anti-inflammatory properties. This study compared the plasma concentrations of interleukins 1-beta (IL-1β), 6 (IL-6), 10 (IL-10), tumor necrosis factor alpha (TNF-α) and irisin in response to intense swimming between adolescent and adult male swimmers. Thirty-two swimmers (16 adolescents, 14 ± 1 years; 16 adults, 21.5 ± 3.1 years) completed a high intensity interval swimming trial. At rest, only TNF-α was higher (33%, p < 0.05) in adolescents compared with adults. There was an overall significant increase in IL-1β from pre- to post-swimming (3% in adolescents, 24% in adults), but no significant interaction. IL-10 significantly increased in both groups (+34% in adolescents, +56% in adults). IL-6 and TNF-α increased significantly (+32% and +26%, respectively) in adults, but not in adolescents (+2% and -9%, respectively). Adults showed a small, but significant decrease in irisin (-5%), with no change in adolescents. The lack of an IL-6, TNF-α and irisin response to intense swimming in adolescent swimmers may suggest a blunted inflammatory and myokine response following high intensity exercise in trained youth.

Keywords: athletes; boys; high-intensity interval exercise; inflammation; men.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Percent changes (Δ mean ± standard error) from pre- to post-swimming in plasma concentrations of interleukin 1-beta (IL-1β), interleukin 6 (IL-6), interleukin 10 (IL-10), tumor necrosis factor alpha (TNF-α) and irisin in adolescent and adult male swimmers. * denotes a significant difference between groups (group effect, p < 0.05). ✧ denotes a significant change from pre- to post-swimming in both groups (time effect, p < 0.05). # denotes a significant change from pre- to post-swimming in adults (interaction, p < 0.05).

References

    1. Nieman D.C., Wentz L.M. The compelling link between physical activity and the body’s defense system. J. Sport Health Sci. 2019;8:201–217. doi: 10.1016/j.jshs.2018.09.009.
    1. Suzuki K. Cytokine Response to Exercise and Its Modulation. Antioxidants. 2018;7:17. doi: 10.3390/antiox7010017.
    1. Bar-Or O. Pediatric Sports Medicine for the Practitioner: From Physiological Principles to Clinical Applications. Springer; New York, NY, USA: 1983.
    1. Falk B., Dotan R. Child-Adult Differences in the Recovery from High-Intensity Exercise. Exerc. Sport Sci. Rev. 2006;34:107–112. doi: 10.1249/00003677-200607000-00004.
    1. Yang W., Hu P. Skeletal muscle regeneration is modulated by inflammation. J. Orthop. Transl. 2018;13:25–32. doi: 10.1016/j.jot.2018.01.002.
    1. Ostrowski K., Rohde T., Asp S., Schjerling P., Pedersen B.K. Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J. Physiol. 1999;515:287–291. doi: 10.1111/j.1469-7793.1999.287ad.x.
    1. Zaldivar F., Wang-Rodriguez J., Nemet D., Schwindt C., Galassetti P., Mills P.J., Wilson L.D., Cooper D.M. Constitutive Pro- and Anti-Inflammatory Cytokine and Growth Factor Response to Exercise in Leukocytes. J. Appl. Physiol. 2006;100:1124–1133. doi: 10.1152/japplphysiol.00562.2005.
    1. Zwetsloot K.A., John C.S., Lawrence M.M., Battista R.A., Shanely R.A. High-intensity interval training induces a modest systemic inflammatory response in active, young men. J. Inflamm. Res. 2014;7:9–17. doi: 10.2147/JIR.S54721.
    1. Timmons B.W., Tarnopolsky M.A., Bar-Or O. Immune Responses to Strenuous Exercise and Carbohydrate Intake in Boys and Men. Pediatr. Res. 2004;56:227–234. doi: 10.1203/01.PDR.0000132852.29770.C5.
    1. Nemet D., Oh Y., Kim H.-S., Hill M., Cooper D.M. Effect of Intense Exercise on Inflammatory Cytokines and Growth Mediators in Adolescent Boys. Pediatrics. 2002;110:681–689. doi: 10.1542/peds.110.4.681.
    1. Rosa J., Oliver S., Flores R., Graf S., Pontello A., Ibardolaza M., Zaldivar F., Galassetti P.R. Kinetic Profiles of 18 Systemic Pro- and Anti-Inflammatory Mediators During and Following Exercise in Children. J. Pediatr. Endocrinol. Metab. 2007;20:1293–1305. doi: 10.1515/JPEM.2007.20.12.1293.
    1. Scheett T.P., Mills P.J., Ziegler M.G., Stoppani J., Cooper D.M. Effect of Exercise on Cytokines and Growth Mediators in Prepubertal Children. Pediatr. Res. 1999;46:429. doi: 10.1203/00006450-199910000-00011.
    1. Webber L.M., Byrnes W.C., Rowland T.W., Foster V.L. Serum Creatine Kinase Activity and Delayed Onset Muscle Soreness in Prepubescent Children: A Preliminary Study. Pediatr. Exerc. Sci. 1989;1:351–359. doi: 10.1123/pes.1.4.351.
    1. Soares J.M., Mota P., Duarte J.A., Appell H.J. Children Are Less Susceptible to Exercise-Induced Muscle Damage than Adults: A Preliminary Investigation. Pediatr. Exerc. Sci. 1996;8:361–367. doi: 10.1123/pes.8.4.361.
    1. Kaji H. Effects of myokines on bone. BoneKEy Rep. 2016;5:826. doi: 10.1038/bonekey.2016.48.
    1. Mazur-Bialy A.I., Pocheć E., Zarawski M. Anti-Inflammatory Properties of Irisin, Mediator of Physical Activity, Are Connected with TLR4/MyD88 Signaling Pathway Activation. Int. J. Mol. Sci. 2017;18:701. doi: 10.3390/ijms18040701.
    1. Daskalopoulou S.S., Cooke A.B., Gomez Y.-H., Mutter A.F., Filippaios A., Mesfum E.T., Mantzoros C.S. Plasma irisin levels progressively increase in response to increasing exercise workloads in young, healthy, active subjects. Eur. J. Endocrinol. 2014;171:343–352. doi: 10.1530/EJE-14-0204.
    1. Huh J.Y., Siopi A., Mougios V., Park K.H., Mantzoros C.S. Irisin in Response to Exercise in Humans With and Without Metabolic Syndrome. J. Clin. Endocrinol. Metab. 2015;100:E453–E457. doi: 10.1210/jc.2014-2416.
    1. Kraemer R., Shockett P., Webb N., Shah U., Castracane V. A Transient Elevated Irisin Blood Concentration in Response to Prolonged, Moderate Aerobic Exercise in Young Men and Women. Horm. Metab. Res. 2013;46:150–154. doi: 10.1055/s-0033-1355381.
    1. Löffler D., Müller U., Scheuermann K., Friebe D., Gesing J., Bielitz J., Erbs S., Landgraf K., Wagner I.V., Kiess W., et al. Serum Irisin Levels Are Regulated by Acute Strenuous Exercise. J. Clin. Endocrinol. Metab. 2015;100:1289–1299. doi: 10.1210/jc.2014-2932.
    1. Huh J.Y., Mougios V., Kabasakalis A., Fatouros I., Siopi A., Douroudos I.I., Filippaios A., Panagiotou G., Park K.H., Mantzoros C.S. Exercise-Induced Irisin Secretion Is Independent of Age or Fitness Level and Increased Irisin May Directly Modulate Muscle Metabolism Through AMPK Activation. J. Clin. Endocrinol. Metab. 2014;99:E2154–E2161. doi: 10.1210/jc.2014-1437.
    1. Hirose L., Nosaka K., Newton M., Laveder A., Kano M., Peake J., Suzuki K. Changes in inflammatory mediators following eccentric exercise of the elbow flexors. Exerc. Immunol. Rev. 2004;10:75–90.
    1. Nagle E.F., Sanders M.E., Franklin B.A. Aquatic High Intensity Interval Training for Cardiometabolic Health. Am. J. Lifestyle Med. 2016;11:64–76. doi: 10.1177/1559827615583640.
    1. Espersen G.T., Elbaek A., Schmidt-Olsen S., Ejlersen E., Varming K., Grunnet N. Short-term changes in the immune system of elite swimmers under competition conditions: Different immunomodulation induced by various types of sport. Scand. J. Med. Sci. Sports. 2007;6:156–163. doi: 10.1111/j.1600-0838.1996.tb00083.x.
    1. Peake J.M., Neubauer O., Della Gatta P.A., Nosaka K. Muscle damage and inflammation during recovery from exercise. J. Appl. Physiol. 2017;122:559–570. doi: 10.1152/japplphysiol.00971.2016.
    1. McKinlay B.J., Theocharidis A., Adebero T., Kurgan N., Fajardo V.A., Roy B.D., Josse A.R., Logan-Sprenger H.M., Falk B., Klentrou P. Effects of Post-Exercise Whey Protein Consumption on Recovery Indices in Adolescent Swimmers. Int. J. Environ. Res. Public Health. 2020;17:7761. doi: 10.3390/ijerph17217761.
    1. Mirwald R.L., Baxter-Jones A.D.G., Bailey D.A., Beunen G.P. An assessment of maturity from anthropometric measurements. Med. Sci. Sports Exerc. 2002;34:689–694. doi: 10.1097/00005768-200204000-00020.
    1. Van Beaumont W. Evaluation of hemoconcentration from hematocrit measurements. J. Appl. Physiol. 1972;32:712–713. doi: 10.1152/jappl.1972.32.5.712.
    1. Kurgan N., Logan-Sprenger H., Falk B., Klentrou N. Training, Inflammation and Bone Markers in Elite Female Rowers during an Olympic Year. Med. Sci. Sports Exerc. 2018;50:1810–1817. doi: 10.1249/MSS.0000000000001640.
    1. Gokhale R., Chandrashekara S., VasanthaKumar K. Cytokine response to strenuous exercise in athletes and non-athletes—An adaptive response. Cytokine. 2007;40:123–127. doi: 10.1016/j.cyto.2007.08.006.
    1. Kouvelioti R., Kurgan N., Falk B., Ward W.E., Josse A.R., Klentrou P. Cytokine and Sclerostin Response to High-Intensity Interval Running versus Cycling. Med. Sci. Sports Exerc. 2019;51:2458–2464. doi: 10.1249/MSS.0000000000002076.
    1. Timmons B.W. Exercise and Immune Function in Children. Am. J. Lifestyle Med. 2007;1:59–66. doi: 10.1177/1559827606294851.
    1. Kargotich S., Goodman C., Keast D., Morton A.R. The Influence of Exercise-Induced Plasma Volume Changes on the Interpretation of Biochemical Parameters Used for Monitoring Exercise, Training and Sport. Sports Med. 1998;26:101–117. doi: 10.2165/00007256-199826020-00004.
    1. Weinstein Y., Bediz C., Dotan R., Falk B. Reliability of peak-lactate, heart rate, and plasma volume following the Wingate test. Med. Sci. Sports Exerc. 1998;30:1456–1460. doi: 10.1097/00005768-199809000-00017.
    1. Kabasakalis A., Nikolaidis S., Tsalis G., Christoulas K., Mougios V. Effects of sprint interval exercise dose and sex on circulating irisin and redox status markers in adolescent swimmers. J. Sports Sci. 2019;37:827–832. doi: 10.1080/02640414.2018.1530056.
    1. Norheim F., Langleite T.M., Hjorth M., Holen T., Kielland A., Stadheim H.K., Gulseth H.L., Birkeland K.I., Jensen J., Drevon C.A. The effects of acute and chronic exercise on PGC-1α, irisin and browning of subcutaneous adipose tissue in humans. FEBS J. 2013;281:739–749. doi: 10.1111/febs.12619.
    1. Fox J., Rioux B.V., Goulet E.D., Johanssen N.M., Swift D.L., Bouchard D.R., Loewen H., Sénéchal M. Effect of an acute exercise bout on immediate post-exercise irisin concentration in adults: A meta-analysis. Scand. J. Med. Sci. Sports. 2017;28:16–28. doi: 10.1111/sms.12904.

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner