The impact of self-reported psychological stress levels on changes to peripheral blood immune biomarkers in recreational marathon runners during training and recovery

NeuroImmunoModulation

Volumn 20, Issue 3, 2013, Pages 164-176

  Rehm, Kristina E ^a,b   Elci, Okan U ^a,b,c   Hahn, Kathryn ^a,d   Marshall, Gailen D ^a,b  

^a Department of Medicine   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MISSISSIPPI   (United States)

^d Department of Psychology   (United States)

Author keywords

Altered immunity; Cytokines; Marathon training; Stress; T lymphocytes

Indexed keywords

BIOLOGICAL MARKER; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4;

ADULT; ANXIETY; ARTICLE; ASSESSMENT OF HUMANS; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; MALE; MARATHON RUNNER; MENTAL STRESS; PATIENT WORRY; PENN STATE WORRY QUESTIONNAIRE; PERCEIVED STRESS SCALE; PRIORITY JOURNAL; RECREATION; REGULATORY T LYMPHOCYTE; SELF REPORT; STATE TRAIT ANXIETY INVENTORY; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL; TH3 CELL; TRAINING;

EID: 84875665958     PISSN: 10217401     EISSN: 14230216     Source Type: Journal    
DOI: 10.1159/000346795     Document Type: Article

References (50)

1. Klentrou P, Cieslak T, MacNeil M, Vintinner A, Plyley M: Effect of moderate exercise on salivary immunoglobulin A and infection risk in humans. Eur J Appl Physiol 2002; 87: 153-158.
2. Akimoto T, Kumai Y, Akama T, Hayashi E, Murakami H, Soma R, Kuno S, Kono I: Effects of 12 months of exercise training on salivary secretory IgA levels in elderly subjects. Br J Sports Med 2003; 37: 76-79.
3. Gleeson M, Bishop N, Oliveira M, McCauley T, Tauler P, Muhamad AS: Respiratory infection risk in athletes: association with antigenstimulated IL-10 production and salivary IgA secretion. Scand J Med Sci Sports 2012; 22: 410-417.
4. Edwards KM, Burns VE, Reynolds T, Carroll D, Drayson M, Ring C: Acute stress exposure prior to influenza vaccination enhances antibody response in women. Brain Behav Immun 2006; 20: 159-168.
5. Edwards KM, Burns VE, Allen LM, McPhee JS, Bosch JA, Carroll D, Drayson M, Ring C: Eccentric exercise as an adjuvant to influenza vaccination in humans. Brain Behav Immun 2007; 21: 209-217.
6. Dimeo F, Bauer M, Varahram I, Proest G, Halter U: Benefits from aerobic exercise in patients with major depression: a pilot study. Br J Sports Med 2001; 35: 114-117.
7. Knubben K, Reischies FM, Adli M, Schlattmann P, Bauer M, Dimeo F: A randomised, controlled study on the effects of a short-term endurance training programme in patients with major depression. Br J Sports Med 2007; 41: 29-33.
8. Kohut ML, Boehm GW, Moynihan JA: Prolonged exercise suppresses antigen-specific cytokine response to upper respiratory infection. J Appl Physiol 2001; 90: 678-684.
9. Kapasi ZF, McRae ML, Ahmed R: Suppression of viral specific primary T-cell response following intense physical exercise in young but not old mice. J Appl Physiol 2005; 98: 663-671.
10. Nieman DC, Simandle S, Henson DA, Warren BJ, Suttles J, Davis JM, Buckley KS, Ahle JC, Butterworth DE, Fagoaga OR, Nehlsen-Cannarella SL: Lymphocyte proliferative response to 2.5 hours of running. Int J Sports Med 1996; 16: 404-409.
11. Lancaster GI, Halson SL, Khan Q, Drysdale P, Wallace F, Jeukendrup AE, Drayson MT, Gleeson M: Effects of acute exhaustive exercise and chronic exercise training on type 1 and type 2 T lymphocytes. Exerc Immunol Rev 2004; 10: 91-106.
12. Nieman DC, Henson DA, Dumke CL, Lind RH, Shooter LR, Gross SJ: Relationship between salivary IgA secretion and upper respiratory tract infection following a 160-km race. J Sports Med Phys Fitness 2006; 46: 158-162.
13. Fahlman MM, Engels HJ: Mucosal IgA and URTI in American college football players: a year longitudinal study. Med Sci Sports Exerc 2005; 37: 374-380.
14. Gleeson M, Pyne DB, Callister R: The missing links in exercise effects on mucosal immunity. Exerc Immunol Rev 2004; 10: 107-128.
15. Nieman DC, Johanssen LM, Lee JW, Arabatzis K: Infectious episodes in runners before and after the Los Angeles Marathon. J Sports Med Phys Fitness 1990; 30: 316-328.
16. Robson-Ansley P, Howatson G, Tallent J, Mitcheson K, Walshe I, Toms C, du Toit G, Smith M, Ansley L: Prevalence of allergy and upper respiratory tract symptoms in runners of the London Marathon. Med Sci Sports Exerc 2012; 44: 999-1004.
17. Running USA: Running USA's Annual Marathon Report. Los Angeles, Running USA, 2012.
18. Steensberg A, Fischer CP, Keller C, Moller K, Pedersen BK: IL6 enhances plasma IL-1ra, IL10, and cortisol in humans. Am J Physiol Endocrinol Metab 2003; 285:E433-E437.
19. Nieman DC, Dumke CL, Henson DA, McAnulty SR, Gross SJ, Lind RH: Muscle damage is linked to cytokine changes following a 160-km race. Brain Behav Immun 2005; 19: 398-403.
20. Pedersen BK: Exercise-induced myokines and their role in chronic diseases. Brain Behav Immun 2011; 25: 811-816.
21. Hall JM, Cruser D, Podawiltz A, Mummert DI, Jones H, Mummert ME: Psychological stress and the cutaneous immune response: roles of the HPA axis and the sympathetic nervous system in atopic dermatitis and psoriasis. Dermatol Res Pract 2012: 403908.
22. Salicru AN, Sams CF, Marshall GD: Cooperative effects of corticosteroids and catecholamines upon immune deviation of the type-1/ type-2 cytokine balance in favor of type-2 expression in human peripheral blood mononuclear cells. Brain Behav Immun 2007; 21: 913-920.
23. Hodgson PD, Aich P, Stookey J, Popowych Y, Potter A, Babiuk L, Griebel PJ: Stress significantly increases mortality following a secondary bacterial respiratory infection. Vet Res 2012; 43: 21.
24. Ashcraft KA, Bonneau RH: Psychological stress exacerbates primary vaginal herpes simplex virus type 1 (HSV-1) infection by impairing both innate and adaptive immune responses. Brain Behav Immun 2008; 22: 1231-1240.
25. Pedersen AF, Zachariae R, Bovbjerg DH: Psychological stress and antibody response to influenza vaccination: a meta-analysis. Brain Behav Immun 2009; 23: 427-433.
26. Uchakin PN, Parish DC, Dane FC, Uchakina ON, Scheetz AP, Agarwal NK, Smith BE: Fatigue in medical residents leads to reactivation of herpes virus latency. Interdiscip Perspect Infect Dis 2011: 571340.
27. Marshall GD, Agarwal SK, Lloyd C, Cohen L, Henninger EM, Morris GJ: Cytokine dysregulation associated with exam stress in healthy medical students. Brain Behav Immun 1998; 12: 297-307.
28. Cohen S, Kamarck T, Mermelstein R: A global measure of perceived stress. J Health Soc Behav 1983; 24: 385-396.
29. Spielberger CD, Gorssuch RL, Lushene PR, Vagg PR, Jacobs GA: Manual for the State-Trait Anxiety Inventory. St. Paul, Consulting Psychologists, 1983.
30. Meyer TJ, Miller ML, Metzger RL, Borkovec TD: Development and validation of the Penn State Worry Questionnaire. Behav Res Ther 1990; 28: 487-495.
31. Beck AT, Ward C, Mendelson M: Beck Depression Inventory. Arch Gen Psychiatry 1961; 4: 561-571.
32. Rehm KE, Xiang L, Elci OU, Griswold M, Marshall GD: Variability in laboratory immune parameters is associated with stress hormone receptor polymorphisms. Neuroimmunomodulation 2012; 19: 220-228.
33. Walsh NP, Gleeson M, Shephard RJ, Gleeson M, Woods JA, Bishop NC, Fleshner M, Green C, Pedersen BK, Hoffman-Goetz L, Rogers CJ, Northoff H, Abbasi A, Simon P: Position statement. Part I: immune function and exercise. Exerc Immunol Rev 2011; 17: 6-63.
34. Zhao G, Zhou S, Davie A, Su Q: Effects of moderate and high intensity exercise on T1/ T2 balance. Exerc Immunol Rev 2012; 18: 98-114.
35. Nieman DC: Marathon training and immune function. Sports Med 2007; 37: 412-415.
36. Lehner T: Special regulatory T cell review: the resurgence of the concept of contrasuppression in immunoregulation. Immunology 2008; 123: 40-44.
37. Lowder T, Dugger K, Deshane J, Estell K, Schwiebert LM: Repeated bouts of aerobic exercise enhance regulatory T cell responses in a murine asthma model. Brain Behav Immun 2010; 24: 153-159.
38. Wang J, Song H, Tang X, Yang Y, Vieira VJ, Niu Y, Ma Y: Effect of exercise training intensity on murine T-regulatory cells and vaccination response. Scand J Med Sci Sports 2011; 22: 643-652.
39. Wilson LD, Zaldivar FP, Schwindt CD, Wang-Rodriguez J, Cooper DM: Circulating T-regulatory cells, exercise and the elite adolescent swimmer. Pediatr Exerc Sci 2009; 21: 305-317.
40. Yeh SH, Chuang H, Lin LW, Hsiao CY, Eng HL: Regular tai chi chuan exercise enhances functional mobility and CD4CD25 regulatory T cells. Br J Sports Med 2006; 40: 239-243.
41. Kim HR, Moon S, Lee HK, Kang JL, Oh S, Seoh JY: Immune dysregulation in chronic stress: a quantitative and functional assessment of regulatory T cells. Neuroimmunomodulation 2012; 19: 187-194.
42. Xiang L, Marshall GD: Immunomodulatory effects of in vitro stress hormones on FoxP3, Th1/Th2 cytokine and costimulatory molecule mRNA expression in human peripheral blood mononuclear cells. Neuroimmunomodulation 2011; 18: 1-10.
43. Xiang L, Del Ben KS, Rehm KE, Marshall GD: Effects of acute stress-induced immunomodulation on Th1/Th2 cytokine and catecholamine receptor expression in human peripheral blood cells. Neuropsychobiology 2012; 65: 12-19.
44. Maddur MS, Miossec P, Kaveri SV, Bayry J: Th17 cells: biology, pathogenesis of autoimmune and inflammatory diseases, and therapeutic strategies. Am J Pathol 2012; 181: 8-18.
45. Czarkowska-Paczek B, Bartlomiejczyk I, Przybylski J: The serum levels of growth factors: PDGF, TGF-beta and VEGF are increased after strenuous physical exercise. J Physiol Pharmacol 2006; 57: 189-197.
46. Mujika I, Padilla S, Pyne D, Busso T: Physiological changes associated with the pre-event taper in athletes. Sports Med 2004; 34: 891-927.
47. Brosschot JF, Pieper S, Thayer JF: Expanding stress theory: prolonged activation and perseverative cognition. Psychoneuroendocrinology 2005; 30: 1043-1049.
48. Borkovec TD, Ray J, Stober J: Worry: a cognitive phenomenon intimately linked to affective physiological, and interpersonal behavioral processes. J Cogn Ther Res 1998; 22: 561-576.
49. Lundeland B, Gundersen Y, Opstad PK, Thrane I, Zhang Y, Olaussen RW, Vaagenes P: One week of multifactorial high-stress military ranger training affects Gram-negative signaling. Scand J Clin Lab Invest 2012; 72: 547-554.
50. Diment BC, Fortes MB, Greeves JP, Casey A, Costa RJ, Walters R, Walsh NP: Effect of daily mixed nutritional supplementation on immune indices in soldiers undertaking an 8-week arduous training programme. Eur J Appl Physiol 2012; 112: 1411-1418.