Journal Mobile Options
Table of Contents
Vol. 20, No. 3, 2013
Issue release date: April 2013
Section title: Original Paper
Neuroimmunomodulation 2013;20:164-176
(DOI:10.1159/000346795)

The Impact of Self-Reported Psychological Stress Levels on Changes to Peripheral Blood Immune Biomarkers in Recreational Marathon Runners during Training and Recovery

Rehm K.E. · Elci O.U. · Hahn K. · Marshall,Jr. G.D.
aLaboratory of Behavioral Immunology Research, bDivision of Clinical Immunology and Allergy, Department of Medicine and cCenter of Biostatistics and Bioinformatics, University of Mississippi Medical Center, and dDepartment of Psychology, Millsaps College, Jackson, Miss., USA

Do you have an account?

Register and profit from personalized services (MyKarger) Login Information

Please create your User ID & Password





Contact Information









I have read the Karger Terms and Conditions and agree.

Register and profit from personalized services (MyKarger) Login Information

Please create your User ID & Password





Contact Information









I have read the Karger Terms and Conditions and agree.

To view the fulltext, please log in

To view the pdf, please log in

Buy

  • FullText & PDF
  • Unlimited re-access via MyKarger (new!)
  • Unrestricted printing, no saving restrictions for personal use
  • Reduced rates with a PPV account
read more

Direct: USD 38.00
Account: USD 26.50

Select

Rent/Cloud

  • Rent for 48h to view
  • Buy Cloud Access for unlimited viewing via different devices
  • Synchronizing in the ReadCube Cloud
  • Printing and saving restriction apply

Rental: USD 8.50
Cloud: USD 20.00

Select

Subscribe

  • Automatic perpetual access to all articles of the subscribed year(s)
  • Unlimited re-access via Subscriber Login or MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

Subcription rates


Select


Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: 11/12/2012 11:28:23 AM
Accepted: 12/21/2012
Published online: 3/27/2013

Number of Print Pages: 13
Number of Figures: 3
Number of Tables: 4

ISSN: 1021-7401 (Print)
eISSN: 1423-0216 (Online)

For additional information: http://www.karger.com/NIM

Abstract

Objective: Marathon training is both physically and psychologically stressful, both of which can lead to altered immunity. The purpose of this study was to determine if the overall immunoregulatory changes associated with the physical stress of marathon training are affected by psychological stress. Methods: Nineteen recreational marathoners completed the Perceived Stress Scale (PSS), State-Trait Anxiety Inventory (STAI) and Penn State Worry Questionnaire (PSWQ), and had levels of T cell subpopulations and cytokine (IFNγ, IL4 and IL10) production determined 4 weeks before (baseline), 24-48 h before (prerace) and 1 week after (recovery) participation in a marathon. Results: PSS scores decreased at the prerace visit compared to baseline and remained low at recovery. Compared to baseline, there were significant changes to numerous immune measures at the prerace visit, including decreases in Th1/Th2 ratio, Tc1/Tc2 ratio, Tr1 and Th3 cell populations as well as decreases in IFNγ/IL4 cytokine ratio and IL10 production. Most immune parameters had returned to near baseline values at the recovery visit. Higher levels of perceived stress, anxiety and worry exacerbated many of the alterations in immunity that were observed at the prerace visit. Higher levels of perceived stress and worry had significant effects on changes to Treg, IL4 production and the IFNγ/IL4 cytokine ratio. Stress had an additional impact on changes in IL10 production. High anxiety levels resulted in significant changes to Treg, Tr1 and Th3. Conclusion: These data suggest that recreational marathon runners with higher levels of psychological stress may be more at risk for the immune alterations that are common during periods of prolonged physical training.


Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: 11/12/2012 11:28:23 AM
Accepted: 12/21/2012
Published online: 3/27/2013

Number of Print Pages: 13
Number of Figures: 3
Number of Tables: 4

ISSN: 1021-7401 (Print)
eISSN: 1423-0216 (Online)

For additional information: http://www.karger.com/NIM


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  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 antigen-stimulated 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.

    External Resources

  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.

    External Resources

  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.

    External Resources

  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.

    External Resources

  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.

    External Resources

  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, Møller K, Pedersen BK: IL6 enhances plasma IL-1ra, IL10, and cortisol in humans. Am J Physiol Endocrinol Metab 2003;285:E433-E437.

    External Resources

  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. Salicrú 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.

    External Resources

  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.

    External Resources

  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.

    External Resources

  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.

    External Resources

  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.

    External Resources

  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.

    External Resources

  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.

    External Resources

  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.