Download PDF
Int J Sports Med 2024; 45(12): 908-916
DOI: 10.1055/a-2338-5397
Physiology & Biochemistry

Kinetics of Immune Cell Mobilization during Acute Aerobic Exercise in Healthy Adults

Frederike Adammek 
1   Division of Performance and Health (Sports Medicine), Department of Sport and Sport Science, TU Dortmund University, Dortmund, Germany
,
Tiffany Y. Wences Chirino
1   Division of Performance and Health (Sports Medicine), Department of Sport and Sport Science, TU Dortmund University, Dortmund, Germany
,
David Walzik 
1   Division of Performance and Health (Sports Medicine), Department of Sport and Sport Science, TU Dortmund University, Dortmund, Germany
,
Sina Trebing
1   Division of Performance and Health (Sports Medicine), Department of Sport and Sport Science, TU Dortmund University, Dortmund, Germany
,
Sergen Belen 
2   Division of Exercise and Movement Science, University of Göttingen Institute for Sport Science, Gottingen, Germany
,
Daniel Renpening
1   Division of Performance and Health (Sports Medicine), Department of Sport and Sport Science, TU Dortmund University, Dortmund, Germany
,
Philipp Zimmer 
1   Division of Performance and Health (Sports Medicine), Department of Sport and Sport Science, TU Dortmund University, Dortmund, Germany
,
Niklas Joisten 
1   Division of Performance and Health (Sports Medicine), Department of Sport and Sport Science, TU Dortmund University, Dortmund, Germany
2   Division of Exercise and Movement Science, University of Göttingen Institute for Sport Science, Gottingen, Germany
› Author Affiliations
› Further Information
Also available at
    Permissions and Reprints

Abstract

While pre-post differences in immune cell mobilization after acute aerobic exercise are well investigated, less is known about when and to what extent immune cells are mobilized during acute aerobic exercise. This experimental trial aimed to investigate the detailed kinetics of circulating immune cells in twelve healthy adults (n=6 females) who completed a 40-min aerobic exercise bout at 60% of the participantsʼ V̇O2peak on a bicycle ergometer. Cellular inflammation markers and sex-dependent differences in circulating immune cells were analyzed. Blood samples were taken immediately before, after warm-up, during exercise after 5 min, 10 min, 15 min, 30 min, 40 min (cessation), and 60 min post exercise. Significant increases in leukocytes (p<0.001), lymphocytes (p<0.001), neutrophils (p=0.003) and platelets (p=0.047) can be observed after 5 min of exercise. The cellular inflammation markers show significant alterations only post exercise. Significant sex differences were observed for neutrophils (p=0.049) and neutrophil-to-lymphocyte ratio (p=0.007) one hour post exercise. These results indicate that i) leukocytes are already mobilized after 5 min of moderate-to-vigorous aerobic exercise, ii) the magnitude of exercise induced leukocyte mobilization is dependent on exercise duration, iii) integrative cellular inflammation markers are only altered after exercise cessation, and iv) the observed effects might be sex-dependent.

Keywords

circulating immune cells - aerobic exercise - NLR - endurance exercise - exercise immunology


Publication History

Received: 15 November 2023

Accepted: 22 May 2024

Accepted Manuscript online:
04 June 2024

Article published online:
19 July 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Gleeson M, Bishop NC, Stensel DJ. et al. The anti-inflammatory effects of exercise: Mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 2011; 11: 607-615
    CrossrefPubMedGoogle Scholar
  • 2 World Health Organization. Global recommendations on physical activity for health. Committee, Guidelines Review (2010.01.01). Internet: https://www.who.int/publications/i/item/9789241599979 status: 2023.06.28
    PubMed
  • 3 Pedersen BK, Saltin B. Exercise as medicine: Evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports 2015; 25: 1-72
    CrossrefPubMedGoogle Scholar
  • 4 Nieman DC, Henson DA, Sampson CS. et al. The acute immune response to exhaustive resistance exercise. Int J Sports Med 1995; 16: 322-328
    Article in Thieme ConnectPubMedGoogle Scholar
  • 5 Campbell JP, Turner JE. Debunking the Myth of Exercise-Induced Immune Suppression: Redefining the Impact of Exercise on Immunological Health Across the Lifespan. Front Immunol 2018; 9: 648
    CrossrefPubMedGoogle Scholar
  • 6 Walsh NP, Gleeson M, Shephard RJ. et al. Position statement. Part one: Immune function and exercise. Exerc Immunol Rev 2011; 17: 6-63
    PubMedGoogle Scholar
  • 7 Simpson RJ, Campbell JP, Gleeson M. et al. Can exercise affect immune function to increase susceptibility to infection?. Exerc Immunol Rev 2020; 26: 8-22
    PubMedGoogle Scholar
  • 8 Pedersen L, Idorn M, Olofsson GH. et al. Voluntary Running Suppresses Tumor Growth through Epinephrine- and IL-6-Dependent NK Cell Mobilization and Redistribution. Cell Metab 2016; 23: 554-562
    CrossrefPubMedGoogle Scholar
  • 9 Krüger K, Mooren FC. T cell homing and exercise. Exerc Immunol Rev 2007; 13: 37-54
    PubMedGoogle Scholar
  • 10 Stojkovic Lalosevic M, Pavlovic Markovic A, Stankovic S. et al. Combined Diagnostic Efficacy of Neutrophil-to-Lymphocyte Ratio (NLR), Platelet-to-Lymphocyte Ratio (PLR), and Mean Platelet Volume (MPV) as Biomarkers of Systemic Inflammation in the Diagnosis of Colorectal Cancer. Dis Markers 2019; 2019: 6036979
    CrossrefPubMedGoogle Scholar
  • 11 Hasselbalch IC, Søndergaard HB, Koch-Henriksen N. et al. The neutrophil-to-lymphocyte ratio is associated with multiple sclerosis. Mult Scler J Exp Trans Clin 2018; 4: 2055217318813183
    PubMedGoogle Scholar
  • 12 Hemond CC, Glanz BI, Bakshi R. et al. The neutrophil-to-lymphocyte and monocyte-to-lymphocyte ratios are independently associated with neurological disability and brain atrophy in multiple sclerosis. BMC Neurol 2019; 19: 23
    CrossrefPubMedGoogle Scholar
  • 13 Zahorec R. Neutrophil-to-lymphocyte ratio, past, present and future perspectives. Bratisl Lek Listy 2021; 122: 474-488
    CrossrefPubMedGoogle Scholar
  • 14 Feng J-F, Chen S, Yang X. Systemic immune-inflammation index (SII) is a useful prognostic indicator for patients with squamous cell carcinoma of the esophagus. Medicine (Baltimore) 2017; 96: e5886
    CrossrefPubMedGoogle Scholar
  • 15 Cai J, Li H, Zhang C. et al. The Neutrophil-to-Lymphocyte Ratio Determines Clinical Efficacy of Corticosteroid Therapy in Patients with COVID-19. Cell Metab 2021; 33: 258-269.e3
    CrossrefPubMedGoogle Scholar
  • 16 Walzik D, Joisten N, Zacher J. et al. Transferring clinically established immune inflammation markers into exercise physiology: Focus on neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio and systemic immune-inflammation index. Eur J Appl Physiol 2021; 121: 1803-1814
    CrossrefPubMedGoogle Scholar
  • 17 Zacher J, Wesemann F, Joisten N. et al. Cellular Integrative Immune Markers in Elite Athletes. Int J Sports Med 2023; 44: 298-308
    Article in Thieme ConnectPubMedGoogle Scholar
  • 18 Wahl P, Mathes S, Bloch W. et al. Acute Impact of Recovery on the Restoration of Cellular Immunological Homeostasis. Int J Sports Med 2020; 41: 12-20
    Article in Thieme ConnectPubMedGoogle Scholar
  • 19 Joisten N, Proschinger S, Rademacher A. et al. High-intensity interval training reduces neutrophil-to-lymphocyte ratio in persons with multiple sclerosis during inpatient rehabilitation. Mult Scler 2021; 27: 1136-1139
    CrossrefPubMedGoogle Scholar
  • 20 Bessa AL, Oliveira VN, Agostini GG. et al. Exercise Intensity and Recovery: Biomarkers of Injury, Inflammation, and Oxidative Stress. J Strength Cond Res 2016; 30: 311-319
    CrossrefPubMedGoogle Scholar
  • 21 Winker M, Stössel S, Neu MA. et al. Exercise reduces systemic immune inflammation index (SII) in childhood cancer patients. Support Care Cancer 2022; 30: 2905-2908
    CrossrefPubMedGoogle Scholar
  • 22 Lee EC, Fragala MS, Kavouras SA. et al. Biomarkers in Sports and Exercise: Tracking Health, Performance, and Recovery in Athletes. J Strength Cond Res 2017; 31: 2920-2937
    CrossrefPubMedGoogle Scholar
  • 23 Fry RW, Morton AR, Crawford GP. et al. Cell numbers and in vitro responses of leucocytes and lymphocyte subpopulations following maximal exercise and interval training sessions of different intensities. Eur J Appl Physiol Occup Physiol 1992; 64: 218-227
    CrossrefPubMedGoogle Scholar
  • 24 Jamurtas AZ, Fatouros IG, Deli CK. et al. The Effects of Acute Low-Volume HIIT and Aerobic Exercise on Leukocyte Count and Redox Status. J Sports Sci Med 2018; 17: 501-508
    PubMedGoogle Scholar
  • 25 Schlagheck ML, Walzik D, Joisten N. et al. Cellular immune response to acute exercise: Comparison of endurance and resistance exercise. Eur J Haematol 2020; 105: 75-84
    CrossrefPubMedGoogle Scholar
  • 26 Nieman DC, Berk LS, Simpson-Westerberg M. et al. Effects of long-endurance running on immune system parameters and lymphocyte function in experienced marathoners. Int J Sports Med 1989; 10: 317-323
    Article in Thieme ConnectPubMedGoogle Scholar
  • 27 Gabriel H, Schwarz L, Born P. et al. Differential mobilization of leucocyte and lymphocyte subpopulations into the circulation during endurance exercise. Eur J Appl Physiol Occup Physiol 1992; 65: 529-534
    CrossrefPubMedGoogle Scholar
  • 28 Galun E, Burstein R, Assia E. et al. Changes of white blood cell count during prolonged exercise. Int J Sports Med 1987; 8: 253-255
    Article in Thieme ConnectPubMedGoogle Scholar
  • 29 Bull FC, Maslin TS, Armstrong T. Global physical activity questionnaire (GPAQ): Nine country reliability and validity study. J Phys Act Health 2009; 6: 790-804
    CrossrefPubMedGoogle Scholar
  • 30 Neves PRDS, Tenório TRDS, Lins TA. et al. Acute effects of high- and low-intensity exercise bouts on leukocyte counts. J Exerc Sci Fit 2015; 13: 24-28
    CrossrefPubMedGoogle Scholar
  • 31 Hill EE, Zack E, Battaglini C. et al. Exercise and circulating cortisol levels: The intensity threshold effect. J Endocrinol Invest 2008; 31: 587-591
    CrossrefPubMedGoogle Scholar
  • 32 Peake JM, Neubauer O, Della Gatta PA. et al. Muscle damage and inflammation during recovery from exercise. J Appl Physiol (1985) 2017; 122: 559-570
    CrossrefPubMedGoogle Scholar
  • 33 Simpson RJ, Kunz H, Agha N. et al. Exercise and the Regulation of Immune Functions. Prog Mol Biol Transl Sci 2015; 135: 355-380
    CrossrefPubMedGoogle Scholar
  • 34 Gustafson MP, Wheatley-Guy CM, Rosenthal AC. et al. Exercise and the immune system: Taking steps to improve responses to cancer immunotherapy. J Immunother Cancer. 2021 9. e001872
    PubMedGoogle Scholar
  • 35 Emery A, Moore S, Crowe J. et al. The effects of short-term, progressive exercise training on disease activity in smouldering multiple myeloma and monoclonal gammopathy of undetermined significance: A single-arm pilot study. BMC Cancer 2024; 24: 174
    CrossrefPubMedGoogle Scholar
  • 36 Emery A, Moore S, Turner JE. et al. Reframing How Physical Activity Reduces The Incidence of Clinically-Diagnosed Cancers: Appraising Exercise-Induced Immuno-Modulation As An Integral Mechanism. Front Oncol 2022; 12: 788113
    CrossrefPubMedGoogle Scholar
  • 37 Joisten N, Walzik D, Schenk A. et al. Aqua cycling for immunological recovery after intensive, eccentric exercise. Eur J Appl Physiol 2019; 119: 1369-1375
    CrossrefPubMedGoogle Scholar
  • 38 Ortega E. The “bioregulatory effect of exercise” on the innate/inflammatory responses. J Physiol Biochem 2016; 72: 361-369
    CrossrefPubMedGoogle Scholar
  • 39 Pennell LM, Galligan CL, Fish EN. Sex affects immunity. J Autoimmun 2012; 38: J282-J291
    CrossrefPubMedGoogle Scholar
  • 40 Nieman DC, Henson DA, Fagoaga OR. et al. Change in salivary IgA following a competitive marathon race. Int J Sports Med 2002; 23: 69-75
    Article in Thieme ConnectPubMedGoogle Scholar
  • 41 Moyna NM, Acker GR, Fulton JR. et al. Lymphocyte function and cytokine production during incremental exercise in active and sedentary males and females. Int J Sports Med 1996; 17: 585-591
    Article in Thieme ConnectPubMedGoogle Scholar
  • 42 Timmons BW, Hamadeh MJ, Devries MC. et al. Influence of gender, menstrual phase, and oral contraceptive use on immunological changes in response to prolonged cycling. J Appl Physiol (1985) 2005; 99: 979-985
    CrossrefPubMedGoogle Scholar
  • 43 Klein SL, Flanagan KL. Sex differences in immune responses. Nat Rev Immunol 2016; 16: 626-638
    CrossrefPubMedGoogle Scholar
  • 44 Poderoso R, Cirilo-Sousa M, Júnior A. et al. Gender Differences in Chronic Hormonal and Immunological Responses to CrossFit. Int J Environ Res Public Health. 2019 16. 2577
    PubMedGoogle Scholar
  • 45 Heaney JLJ, Carroll D, Phillips ACDHEA. DHEA-S and cortisol responses to acute exercise in older adults in relation to exercise training status and sex. Age (Dordr) 2013; 35: 395-405
    CrossrefPubMedGoogle Scholar