Download PDF
Int J Sports Med 2024; 45(03): 245-252
DOI: 10.1055/a-2186-2717
Clinical Sciences

Immunometabolic and Vascular Health Responses among High Endurance Trained Subjects

Henrique A.R. Fonseca 
1   Cardiology Division, Department of Medicine, Federal University of Sao Paulo, São Paulo, SP, Brazil
2   Department of Immunology, Institute Biomedical Science IV, University of Sao Paulo, São Paulo, SP, Brazil
3   National Institute of Technology in Complex Fluids, Physics Institute, University of Sao Paulo, São Paulo, SP, Brazil
,
Celia Regina Bittencourt
1   Cardiology Division, Department of Medicine, Federal University of Sao Paulo, São Paulo, SP, Brazil
,
Andrea Moreira Monteiro
2   Department of Immunology, Institute Biomedical Science IV, University of Sao Paulo, São Paulo, SP, Brazil
3   National Institute of Technology in Complex Fluids, Physics Institute, University of Sao Paulo, São Paulo, SP, Brazil
,
Francisco Antonio Fonseca
1   Cardiology Division, Department of Medicine, Federal University of Sao Paulo, São Paulo, SP, Brazil
3   National Institute of Technology in Complex Fluids, Physics Institute, University of Sao Paulo, São Paulo, SP, Brazil
,
Lívia Rentas Sanches
4   Hospital Israelita Albert Einstein, São Paulo, SP, Brazil
,
Carlos Eduardo dos Santos Ferreira
4   Hospital Israelita Albert Einstein, São Paulo, SP, Brazil
,
Antonio Martins Figueiredo Neto
3   National Institute of Technology in Complex Fluids, Physics Institute, University of Sao Paulo, São Paulo, SP, Brazil
,
Magnus Gidlund
2   Department of Immunology, Institute Biomedical Science IV, University of Sao Paulo, São Paulo, SP, Brazil
,
Maria Cristina Izar
1   Cardiology Division, Department of Medicine, Federal University of Sao Paulo, São Paulo, SP, Brazil
3   National Institute of Technology in Complex Fluids, Physics Institute, University of Sao Paulo, São Paulo, SP, Brazil
› Author Affiliations Funding Informationen This is study was supported by the National Council of Technological and Scientific Development (CNPq). HARF was supported by a fellowship grant from the National Institute of Science and Technology in Complex Fluids (INCT-Fcx) process 157872/2013–0. HARF and MG received a research grant from São Paulo Research Foundation (FAPESP) (Grant number: 2021/08111–2).
› Further Information
Also available at
   Permissions and Reprints

Abstract

In this study, we aimed to examine the impact of high endurance training on vascular health parameters and immune-endocrine responses against modified low-density lipoprotein (LDL) particles. This observational, cross-sectional study included high endurance-trained and healthy non-trained subjects. Vascular ultrasound was used to assess vascular health parameters based on carotid intima-media thickness and endothelial function (flow-mediated dilation). Enzyme-linked immunosorbent assays were used to measure interleukin (IL)-8 and IL-10, autoantibody isotypes anti-oxidized LDL (oxLDL) and anti-apolipoprotein B (ApoB-D) peptide. Plasma levels of the corticosterone and 17 α-hydroxyprogesterone hormones were analyzed by mass spectrometry. This study enrolled 96 subjects, of whom 44 were high endurance trained and 52 were healthy non-trained individuals. Smaller carotid intima-media thickness values were observed in the high-endurance trained than in the healthy non-trained males, while no differences were observed between female groups. Flow-mediated dilation measurements did not differ by training or sex. The humoral immune responses to IgG anti-oxLDL and IgM anti-ApoB-D autoantibodies showed an isotype imbalance between the high-endurance trained and the non-trained groups. Immunoendocrine parameters showed inverse correlations between 17 α-hydroxyprogesterone concentrations and carotid intima-media thickness measurements. Direct correlations were found between IL-10 concentrations and flow-mediated dilation measurements. Chronic high-endurance exercise modulates immune-endocrine and vascular health parameters, in a sex-dependent manner.

Key words

exercise - humoral immunity - oxidized LDL - atherosclerosis - endothelium


Publication History

Received: 09 July 2023

Accepted: 02 October 2023

Accepted Manuscript online:
04 October 2023

Article published online:
22 December 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Lee DC, Pate RR, Lavie CJ. et al. Leisure-time running reduces all-cause and cardiovascular mortality risk. J Am Coll Cardiol 2014; 64: 472-481
    CrossrefPubMedSearch in Google Scholar
  • 2 Wen CP, Wai JP, Tsai MK. et al. Minimum amount of physical activity for reduced mortality and extended life expectancy: A prospective cohort study. Lancet 2011; 378: 1244-1253
    CrossrefPubMedSearch in Google Scholar
  • 3 Kadoglou NP, Moustardas P, Kapelouzou A. et al. The anti-inflammatory effects of exercise training promote atherosclerotic plaque stabilization in apolipoprotein E knockout mice with diabetic atherosclerosis. Eur J Histochem: EJH 2013; 57: e3
    CrossrefPubMedSearch in Google Scholar
  • 4 Napoli C, Williams-Ignarro S, De Nigris F. et al. Long-term combined beneficial effects of physical training and metabolic treatment on atherosclerosis in hypercholesterolemic mice. Proc Natl Acad Sci USA 2004; 101: 8797-8802
    CrossrefPubMedSearch in Google Scholar
  • 5 Kadoglou NP, Iliadis F, Liapis CD. Exercise and carotid atherosclerosis. Eur J Vasc Endovasc Surg 2008; 35: 264-272
    CrossrefPubMedSearch in Google Scholar
  • 6 Taylor BA, Zaleski AL, Capizzi JA. et al. Influence of chronic exercise on carotid atherosclerosis in marathon runners. BMJ Open 2014; 4: e004498
    CrossrefPubMedSearch in Google Scholar
  • 7 Radak Z, Zhao Z, Koltai E. et al. Oxygen consumption and usage during physical exercise: The balance between oxidative stress and ROS-dependent adaptive signaling. Antioxid Redox Signal. 2013 18. 1208-1246
    PubMedSearch in Google Scholar
  • 8 Ashor AW, Lara J, Siervo M. et al. Exercise modalities and endothelial function: A systematic review and dose-response meta-analysis of randomized controlled trials. Sports Med 2015; 45: 279-296
    CrossrefPubMedSearch in Google Scholar
  • 9 Kosola J, Ahotupa M, Kyröläinen H. et al. Young men with poor cardiorespiratory fitness combined with lower testosterone have high levels of oxidized LDL lipids – a being fit alters this relationship. Int J Sport Nutr Exerc Metab 2013; 23: 629-637
    CrossrefPubMedSearch in Google Scholar
  • 10 Rhibi F, Zouhal H, Lira FS. et al. Inflammatory cytokines and metabolic responses to high-intensity intermittent training: Effect of the exercise intensity. Biol Sport 2022; 39: 263-272
    CrossrefPubMedSearch in Google Scholar
  • 11 Castanho VS, Gidlund M, Nakamura R. et al. Post-menopausal hormone therapy reduces autoantibodies to oxidized apolipoprotein B100. Gynecol Endocrinol 2011; 27: 800-806
    CrossrefPubMedSearch in Google Scholar
  • 12 Dhayni K, Zibara K, Issa H. et al. Targeting CXCR1 and CXCR2 receptors in cardiovascular diseases. Pharmacol Ther 2022; 237: 108257
    CrossrefPubMedSearch in Google Scholar
  • 13 Gleeson M, Bishop N, Oliveira M. et al. Influence of training load on upper respiratory tract infection incidence and antigen-stimulated cytokine production. Scand J Med Sci Sports 2013; 23: 451-457
    CrossrefPubMedSearch in Google Scholar
  • 14 Buchfuhrer MJ, Hansen JE, Robinson TE. et al. Optimizing the exercise protocol for cardiopulmonary assessment. J Appl Physiol 1983; 55: 1558-1564
    CrossrefPubMedSearch in Google Scholar
  • 15 Neder JA, Stein RA. Simplified strategy for the estimation of the exercise ventilator thresholds. Med Sci Sports Exerc 2006; 38: 1007-1013
    CrossrefPubMedSearch in Google Scholar
  • 16 Corretti MC, Anderson TJ, Benjamin EJ. et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery. a report of the international brachial artery reactivity task force. J Am Coll Cardiol 2002; 39: 257-265
    CrossrefPubMedSearch in Google Scholar
  • 17 Stein JH, Korcarz CE, Hurst RT. et al. American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: A consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force. Endorsed by the Society for Vascular Medicine. J Am Soc Echocardiogr 2008; 21: 93-111
    CrossrefPubMedSearch in Google Scholar
  • 18 Zaratin A, Gidlund M, Boschcov P. et al. Antibodies against oxidized low-density lipoprotein in normolipidemic smokers. Am J Cardiol 2002; 90: 651-653
    CrossrefPubMedSearch in Google Scholar
  • 19 Izar MC, Fonseca HA, Pinheiro LF. et al. Adaptive immunity is related to coronary artery disease severity after acute coronary syndrome in subjects with metabolic syndrome. Diab Vasc Dis Res 2013; 10: 32-39
    CrossrefPubMedSearch in Google Scholar
  • 20 Fernvik EC, Ketelhuth DF, Russo M. et al. The autoantibody repertoire against copper- or macrophage-modified LDL differs in normolipidemics and hypercholesterolemic patients. J Clin Immunol 2004; 24: 170-176
    CrossrefPubMedSearch in Google Scholar
  • 21 da Fonseca HA, Fonseca FA, Monteiro AM. et al. Inflammatory environment and immune responses to oxidized LDL are linked to systolic and diastolic blood pressure levels in hypertensive subjects. Int J Cardiol 2012; 157: 131-133
    CrossrefPubMedSearch in Google Scholar
  • 22 Cook CJ, Crewther BT, Smith AA. Comparison of baseline free testosterone and cortisol concentrations between elite and non-elite female athletes. Am J Hum Biol 2012; 24: 856-858
    CrossrefPubMedSearch in Google Scholar
  • 23 Tarkhan AH, Anwardeen NR, Sellami M. et al. Comparing metabolic profiles between female endurance athletes and non-athletes reveals differences in androgen and corticosteroid levels. J Steroid Biochem Mol Biol 2022; 219: 106081
    CrossrefPubMedSearch in Google Scholar
  • 24 Kłapcińska B, Kempa K, Sobczak A. et al. Evaluation of autoantibodies against oxidized LDL (oLAB) and blood antioxidant status in professional soccer players. Int J Sports Med 2005; 26: 71-78
    Thieme ConnectPubMedSearch in Google Scholar
  • 25 Veljkovic M, Dopsaj V, Stringer WW. et al. Aerobic exercise training as a potential source of natural antibodies protective against human immunodeficiency virus-1. Scand J Med Sci Sports 2010; 20: 469-474
    CrossrefPubMedSearch in Google Scholar
  • 26 Gualano B, Lemes IR, Silva RP. et al. Association between physical activity and immunogenicity of an inactivated virus vaccine against SARS-CoV-2 in patients with autoimmune rheumatic diseases. Brain Behav Immun 2022; 101: 49-56
    CrossrefPubMedSearch in Google Scholar
  • 27 Ledo A, Schub D, Ziller C. et al. Elite athletes on regular training show more pronounced induction of vaccine-specific T-cells and antibodies after tetravalent influenza vaccination than controls. Brain Behav Immun 2020; 83: 135-145
    CrossrefPubMedSearch in Google Scholar
  • 28 Fonseca HA, Lins LC, Fonseca FA. et al. Antihypertensive therapy increases innate immune response in hypertensive patients. Life Sci 2015; 143: 124-130
    CrossrefPubMedSearch in Google Scholar
  • 29 Fonseca HA, Fonseca FA, Monteiro AM. et al. Obesity modulates the immune response to oxidized LDL in hypertensive patients. Cell Biochem Biophys 2013; 67: 1451-1460
    CrossrefPubMedSearch in Google Scholar
  • 30 Fagerberg B, Prahl Gullberg U, Alm R. et al. Circulating autoantibodies against the apolipoprotein B-100 peptides p45 and p210 in relation to the occurrence of carotid plaques in 64-year-old women. PLoS One 2015; 10: e0120744
    CrossrefPubMedSearch in Google Scholar
  • 31 Fredrikson GN, Hedblad B, Berglund G. et al. Association between IgM against an aldehyde-modified peptide in apolipoprotein B-100 and progression of carotid disease. Stroke 2007; 38: 1495-1500
    CrossrefPubMedSearch in Google Scholar
  • 32 Svensjö E, Boschcov P, Ketelhuth DF. et al. Increased microvascular permeability in the hamster cheek pouch induced by oxidized low density lipoprotein (oxLDL) and some fragmented apolipoprotein B proteins. Inflamm Res 2003; 52: 215-220
    CrossrefPubMedSearch in Google Scholar
  • 33 Durand MJ, Gutterman DD. Exercise and vascular function: How much is too much?. Can J Physiol Pharmacol 2014; 92: 551-557
    CrossrefPubMedSearch in Google Scholar
  • 34 Wilson MG, Ellison GM, Cable NT. Basic science behind the cardiovascular benefits of exercise. Heart 2015; 101: 758-765
    CrossrefPubMedSearch in Google Scholar
  • 35 Augustine JA, Lefferts WK, Dowthwaite JN. et al. Subclinical atherosclerotic risk in endurance-trained premenopausal amenorrheic women. Atherosclerosis 2016; 244: 157-164
    CrossrefPubMedSearch in Google Scholar
  • 36 Tsiflikas I, Thomas C, Fallmann C. et al. Prevalence of subclinical coronary artery disease in middle-aged, male marathon runners detected by cardiac CT. Rofo 2015; 187: 561-568
    Thieme ConnectPubMedSearch in Google Scholar
  • 37 Fonseca HA, Bittencourt CR, Fonseca FA. et al. Non-linear optical responses of low-density lipoprotein are associated with intima-media thickness of carotid artery in athletes. Cell Biochem Biophys 2016; 74: 253-262
    CrossrefPubMedSearch in Google Scholar
  • 38 Gleeson M, Bishop N, Oliveira M. et al. Influence of training load on upper respiratory tract infection incidence and antigen-stimulated cytokine production. Scand J Med Sci Sports 2013; 23: 451-457
    CrossrefPubMedSearch in Google Scholar