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

Springer Science and Business Media LLC - Tập 97 - Trang 151-157 - 2006
Yngvar Gundersen1, Per Kristian Opstad1, Trine Reistad1, Ingjerd Thrane1, Per Vaagenes1
1Division of Protection, Norwegian Defence Research Establishment, Kjeller, Norway

Tóm tắt

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.

Tài liệu tham khảo

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 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 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 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 Eversen CA, Toth LA (2000) Systemic bacterial invasion induced by sleep deprivation. Am J Physiol 278:R905–R916 Fellmann N (1992) Hormonal and plasma volume alterations following endurance exercise. A brief review. Sports Med 13:37–49 Friese RS, Rehring TF, Wollmering M, Moore EE, Ketch LL, Banerjee A, Harken AH (1994) Trauma primes cells: editorial review. Shock 1:388–394 Gleeson M, Bishop NC (2000) Elite athlete immunology: importance of nutrition. Int J Sports Med 21:S44–S50 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 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 Halson SL, Lancaster GI, Jeukendrup AE, Gleeson M (2003) Immunological responses to overreaching in cyclists. Med Sci Sports Exerc 35:854–861 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 Heath GW, Macer CA, Nieman DC (1992) Exercise and upper respiratory tract infections: is there a relationship? Sports Med 14:353–365 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 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 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 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 Moldoveanu AI, Shephard RJ, Shek PN (2001) The cytokine response to physical activity and training. Sports Med 31:115–144 Nielsen HB, Pedersen BK (1997) Lymphocyte proliferation in response to exercise. Eur J Appl Physiol 75:375–379 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 Nieman DC (2000) Is infection linked to exercise workload? Med Sci Sports Exerc 32:S406–S411 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 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 Pedersen BK (2000) Exercise and cytokines. Immunol Cell Biol 78:532–535 Pedersen BK, Hoffman-Goetz L (2000) Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 80:1055–1081 Pedersen BK, Nieman D (1998) Exercise immunology: integration and regulation. Immunol Today 19:204–206 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 Rowbottom DG, Green KJ (2000) Acute exercise effects on the immune system. Med Sci Sports Exerc 32:S396–S405 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 Shephard RJ, Shek PN (1995) Heavy exercise, nutrition and immune function: is there a connection? Int J Sports Med 16:491–497 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 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 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 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 Wing EJ, Young JB (1980) Acute starvation protects mice against Listeria monocytogenes. Infect Immun 28:771–776