Skip to main content

Advertisement

Log in

Seven days’ around the clock exhaustive physical exertion combined with energy depletion and sleep deprivation primes circulating leukocytes

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Both exhaustive physical exertion and starvation have been reported to induce depression of immune function. The aim of the present study was to investigate the inflammatory environment and state of activation and mediator-producing potential of circulating leukocytes during prolonged physical activity with concomitant energy and sleep deprivation. Eight well-trained males were studied during 7 days of semi-continuous physical activity. Sleep was restricted to about 1 h/24 h, energy intake to 1.5– 3.0 MJ/24 h. Blood was drawn at 07.00 a.m. on days 0, 2, 4, and 7. Plasma levels of inflammation markers were measured. The response of circulating leukocytes to lipopolysaccharide (LPS; 1 μg mL−1), and the effect of added hydrocortisone (10 and 100 nmol L−1), were measured in the supernatant after 3 h of incubation in an ex vivo whole blood model. Activation of leukocytes steadily increased as measured by plasma matrix metalloproteinase-9, tumour necrosis factor-α, interleukin-1β, and interleukin-6. Inhibitors of systemic inflammation were either unaltered (tissue inhibitor of matrix metalloproteinase-1) or elevated (plasma interleukin-1 receptor antagonist). Cortisol levels increased on days 2 and 4, but thereafter reverted to baseline values. The leukocytes responded to LPS activation with increasing release of inflammatory cytokines throughout the study period. The anti-inflammatory potency of hydrocortisone decreased. Prolonged multifactorial stress thus activated circulating immune cells and primed them for an increased response to a subsequent microbial challenge.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bøyum A, Wiik P, Gustavsson E, Veiby OP, Reseland J, Haugen A-H, Opstad PK (1996) The effect of strenuous exercise, calorie deficiency and sleep deprivation on white blood cell, plasma immunoglobulins and cytokines. Scand J Immunol 43:228–235

    Article  PubMed  Google Scholar 

  • Chan J, Tian Y, Tanaka KE, Tsang MS, Yu K, Salgame P, Carroll D, Kress Y, Teitelbaum R, Bloom BR (1996) Effects of protein calorie malnutrition on tuberculosis in mice. Proc Natl Acad Sci USA 93:14857–14861

    Article  PubMed  CAS  Google Scholar 

  • Dill DB, Costill DL (1974) Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J Appl Physiol 37:247–248

    PubMed  CAS  Google Scholar 

  • Dinges DF, Douglas SD, Zaugg L, Campbell DE, McMann JM, Whitehouse WG, Orne EC, Kapoor SC, Icaza E, Orne MT (1994) Leukocytosis and natural killer cell function parallel neurobehavioral fatigue induced by 64 hours of sleep deprivation. J Clin Invest 93:1930–1939

    Article  PubMed  CAS  Google Scholar 

  • Eversen CA, Toth LA (2000) Systemic bacterial invasion induced by sleep deprivation. Am J Physiol 278:R905–R916

    Google Scholar 

  • Fellmann N (1992) Hormonal and plasma volume alterations following endurance exercise. A brief review. Sports Med 13:37–49

    CAS  Google Scholar 

  • Friese RS, Rehring TF, Wollmering M, Moore EE, Ketch LL, Banerjee A, Harken AH (1994) Trauma primes cells: editorial review. Shock 1:388–394

    Article  PubMed  CAS  Google Scholar 

  • Gleeson M, Bishop NC (2000) Elite athlete immunology: importance of nutrition. Int J Sports Med 21:S44–S50

    Article  PubMed  CAS  Google Scholar 

  • Goldberg AC, Eliaschewitz FG, Montor WR, Baracho GV, Errante PR, Callero MA, Cardoso MR, Braga PE, Kalil J, Sogayar MC, Rizzo LV (2005) Exogenous leptin restores in vitro T-cell proliferation and cytokine synthesis in patients with common variable immunodeficiency syndrome. Clin Immunol 114:147–153

    Article  PubMed  CAS  Google Scholar 

  • Gundersen Y, Vaagenes P, Thrane I, Bogen IL, Haug KH, Reistad T, Opstad PK (2005) Response of circulating immune cells to major gunshot injury, haemorrhage, and acute surgery. Injury 36:949–955

    Article  PubMed  CAS  Google Scholar 

  • Halson SL, Lancaster GI, Jeukendrup AE, Gleeson M (2003) Immunological responses to overreaching in cyclists. Med Sci Sports Exerc 35:854–861

    Article  PubMed  Google Scholar 

  • Heagy W, Nieman K, Hansen C, Cohen D, Danielson M, West MA (2003) Lower levels of whole blood LPS-stimulated cytokine release are associated with poorer clinical outcomes in surgical ICU patients. Surg Infect 4:171–180

    Article  Google Scholar 

  • Heath GW, Macer CA, Nieman DC (1992) Exercise and upper respiratory tract infections: is there a relationship? Sports Med 14:353–365

    Article  PubMed  CAS  Google Scholar 

  • Irwin M, McClintick J, Costlow C, Fortner M, White J, Gillin JC (1996) Partial night sleep deprivation reduces natural killer and cellular immune responses in humans. FASEB J 10:643–653

    PubMed  CAS  Google Scholar 

  • Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI (1998) Leptin modulates the T-cell immune responses and reverses starvation-induced immunosuppression. Nature 394:897–901

    Article  PubMed  CAS  Google Scholar 

  • Lundvall J, Bjerkhoel P (1995) Pronounced and rapid plasma volume reduction upon quiet standing as revealed by a novel approach to the determination of the intravascular volume change. Acta Physiol Scand 154:131–142

    Article  PubMed  CAS  Google Scholar 

  • Marable NL, Hickson JF, Korslund MK, Herbert WG, Desjardins RF, Thye FW (1979) Urinary nitrogen excretion as influenced by muscle building. Exercise program and protein intake variation. Nutr Rep Int 19:795–805

    CAS  Google Scholar 

  • Moldoveanu AI, Shephard RJ, Shek PN (2001) The cytokine response to physical activity and training. Sports Med 31:115–144

    Article  PubMed  CAS  Google Scholar 

  • Nielsen HB, Pedersen BK (1997) Lymphocyte proliferation in response to exercise. Eur J Appl Physiol 75:375–379

    Article  CAS  Google Scholar 

  • Nielsen HG, Hagberg IA, Lyberg T (2004) Marathon running leads to partial exhaustion of ROS-generating capacity in leukocytes. Med Sci Sports Exercise 36:68–73

    Article  CAS  Google Scholar 

  • Nieman DC (2000) Is infection linked to exercise workload? Med Sci Sports Exerc 32:S406–S411

    Article  PubMed  CAS  Google Scholar 

  • Nieman DC, Henson DA, Smith LL, Utter AC, Vinci DM, Davis JM, Kaminsky DE, Shute M (2001) Cytokine changes after a marathon race. J Appl Physiol 91:109–114

    PubMed  CAS  Google Scholar 

  • Opstad PK (1995) Medical consequences in young men of prolonged physical stress with sleep and energy deficiency. Norwegian Defence Research Establishment /Publication-95/05586, Kjeller, Norway

  • Pasquale MD, Cipolle MD, Monaco J, Simon N (1996) Early inflammatory response correlates with the severity of injury. Crit Care Med 24:1238–1242

    Article  PubMed  CAS  Google Scholar 

  • Pedersen BK (2000) Exercise and cytokines. Immunol Cell Biol 78:532–535

    Article  PubMed  CAS  Google Scholar 

  • Pedersen BK, Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 80:1055–1081

    PubMed  CAS  Google Scholar 

  • Pedersen BK, Nieman D (1998) Exercise immunology: integration and regulation. Immunol Today 19:204–206

    Article  PubMed  CAS  Google Scholar 

  • Pedersen BK, Bruunsgaard H, Klokker M, Kappel M, MacLean DA, Nielsen HB, Rohde T, Ullum H, Zacho M (1997) Exercise-induced immunomodulation – possible roles of neuroendocrine and metabolic factors. Int J Sports Med 18(suppl 1):2–7

    Article  Google Scholar 

  • Rowbottom DG, Green KJ (2000) Acute exercise effects on the immune system. Med Sci Sports Exerc 32:S396–S405

    Article  PubMed  CAS  Google Scholar 

  • Sarraf P, Frederich RC, Turner EM, Ma G, Jaskowiak NT, Rivet DJ, Flier JS, Lowell BB, Fraker DL, Alexander HR (1997) Multiple cytokines and acute inflammation raise mouse leptin levels: potential role in inflammatory anorexia. J Exp Med 185:171–175

    Article  PubMed  CAS  Google Scholar 

  • Shephard RJ, Shek PN (1995) Heavy exercise, nutrition and immune function: is there a connection? Int J Sports Med 16:491–497

    Article  PubMed  CAS  Google Scholar 

  • Smith JA, Gray AB, Pyne DB, Baker MS, Telford RD, Weidemann MJ (1996) Moderate exercise triggers both priming and activation of neutrophil subpopulations. Am J Physiol 270:R838–R845

    PubMed  CAS  Google Scholar 

  • Smits HH, Grünberg K, Derijk RH, Sterk PJ, Hiemstra PS (1998) Cytokine release and its modulation by dexamethasone in whole blood following exercise. Clin Exp Immunol 111:463–468

    Article  PubMed  CAS  Google Scholar 

  • Steensberg A, van Hall G, Osada T, Sacchetti M, Saltin B, Pedersen BK (2000) Production of interleukin-6 in contracting human skeletal muscles can account for the execise-induced increase in plasma interleukin-6. J Physiol 529:237–242

    Article  PubMed  CAS  Google Scholar 

  • Suzuki K, Yamada M, Kurakake S, Okamura N, Yamaya K, Liu Q, Kudoh S, Kowatari K, Nakaji S, Sugawara K (2000) Circulating cytokines and hormones with immunosuppressive but neutrophil-priming potentials rise after endurance exercise in humans. Eur J Appl Physiol 81:281–287

    Article  PubMed  CAS  Google Scholar 

  • Wing EJ, Young JB (1980) Acute starvation protects mice against Listeria monocytogenes. Infect Immun 28:771–776

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank the cadets at the Norwegian Military Academy who volunteered to take part in this study and thus were exposed to additional strain.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yngvar Gundersen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gundersen, Y., Opstad, P.K., Reistad, T. et al. Seven days’ around the clock exhaustive physical exertion combined with energy depletion and sleep deprivation primes circulating leukocytes . Eur J Appl Physiol 97, 151–157 (2006). https://doi.org/10.1007/s00421-006-0150-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-006-0150-8

Keywords

Navigation