Relationships between inflammatory cytokine and cortisol responses in firefighters exposed to simulated wildfire suppression work and sleep restriction

Physiological Reports

Volumn 3, Issue 11, 2015, Pages

  Wolkow, Alexander ^a,b   Aisbett, Brad ^a,b   Reynolds, John ^c   Ferguson, Sally A ^b,d   Main, Luana C ^a  

^a DEAKIN UNIVERSITY   (Australia)

^b BUSHFIRE COOPERATIVE RESEARCH CENTRE   (Australia)

^c DEAKIN UNIVERSITY   (Australia)

^d CENTRAL QUEENSLAND UNIVERSITY   (Australia)

Author keywords

Cortisol; cytokines; firefighters; physical work; sleep restriction

Indexed keywords

EID: 84965077994     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12604     Document Type: Article

References (92)

1. Abedelmalek, S., N. Souissi, H. Chtourou, M. Denguezli, C. Aouichaoui, M. Ajina, et al. 2013. Effects of partial sleep deprivation on proinflammatory cytokines, growth hormone, and steroid hormone concentrations during repeated brief sprint interval exercise. Chronobiol. Int. 30:502–509.
2. Aisbett, B., M. Phillips, J. Raines, and D. Nichols. 2007. Work patterns of tanker-based bushfire suppression by Australian volunteer firefighters in south-east Australia. Human Dimensions of Wildfire Conference, Fort Collins, Colorado.
3. Aisbett, B., A. Wolkow, M. Sprajcer, and S. A. Ferguson. 2012. “Awake, smoky, and hot”: providing an evidence-base for managing the risks associated with occupational stressors encountered by wildland firefighters. Appl. Ergon. 43:916–925.
4. Al-Malki, A. L., A. M. Rezq, and M. H. Al-Saedy. 2008. Effect of fire smoke on some biochemical parameters in firefighters of Saudi Arabia. J. Occup. Med. Toxicol. 3. doi: 10.1186/1745-6673-3-33.
5. An, S. J., Y. K. Chung, B. H. Kim, K. M. Kwak, J. S. Son, J. W. Koo, et al. 2015. The effect of organisational system on self-rated depression in a panel of male municipal firefighters. Ann. Occup. Environ. Med. 27:1–7.
6. Appel, C. P., A. C. Blomkvist, L. O. Persson, and L. Sjöberg. 1980. Mood and achievement in a difficult driving task. Ergonomics 23:605–612.
7. Biopharmaceutics Coordinating Committee 2001. Bioanalytical method validation. Pp. 1–22 in U.S. Department of health and human services food and drug administration & Center for Drug Evaluation and Research (CDER), ed. Guidance for industry. Center for Veterinary Medicine (CVM), United States Department of Health and Human Services Food and Drug Administration, Silver Spring, MD.
8. Bøyum, A., P. Wiik, E. Gustavsson, O. P. Veiby, J. Reseland, A. H. Haugen, et al. 1996. The effect of strenuous exercise, calorie deficiency and sleep deprivation on white blood cells, plasma immunoglobulins and cytokines. Scand. J. Immunol. 43:228–235.
9. Budd, G. M., J. R. Brotherhood, A. L. Hendrie, S. E. Jeffery, F. A. Beasley, B. P. Costin, et al. 1997. Project Aquarius 4. Experimental bushfires, suppression procedures, and measurements. Int. J. Wildl. Fire 7:99–104.
10. Burgess, J. L., C. J. Nanson, T. A. Hysong, R. Gerkin, M. L. Witten, and R. C. Lantz. 2002. Rapid decline in sputum IL-10 concentration following occupational smoke exposure. Inhalation Toxicol. 14:133–140.
11. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multi-model inference: a practical information-theoretic approach/Kenneth P. Burnham, David R. Anderson. Springer, London, U.K.
12. Carey, M. G., S. S. Al-Zaiti, G. E. Dean, L. Sessanna, and D. S. Finnell. 2011. Sleep problems, depression, substance use, social bonding, and quality of life in professional firefighters. J. Occup. Environ. Med. 53:928–933.
13. Carlson, M., V. Charlin, and N. Miller. 1988. Positive mood and helping behavior: a test of six hypotheses. J. Pers. Soc. Psychol. 55:211–229.
14. Cater, H., D. Clancy, K. Duffy, A. Holgate, B. Wilison, and J. Wood. 2007. Fatigue on the fireground: the DPI experience. Pp. 1–6 in R. Thornton, ed. Bushfire cooperative research centre/Australasian fire authorities council conference research forum. Bushfire Cooperative Research Centre, Hobart, Tasmania.
15. Chowdhury, F., A. Williams, and P. Johnson. 2009. Validation and comparison of two multiplex technologies, Luminex and Mesoscale Discovery, for human cytokine profiling. J. Immunol. Methods 340:55–64.
16. Christoforou, T., M. Cvirn, S. Ferguson, T. Armstrong, and B. Smith. 2013. The effect of sleep restriction and exposure to physical activity on the cognitive ability of volunteer firefighters across a 3-day simulated fire-ground tour. Pp. 13–17 in C. Sargent and X. Zhou, eds. Sleep. Performance and Wellbeing in Adults and Adolescents. Australasian Chronobiology Society, Adelaide.
17. Chrousos, G. P. 1995. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation. N. Engl. J. Med. 332:1351–1362.
18. Cook, B., and W. Mitchell. 2013. Occupational health effects for firefighters: the extent and implications of physical and psychological injuries. Centre of Full Employment and Equity, Melbourne.
19. Corsini, E., A. Pinto, V. Galbiati, B. Viviani, C. L. Galli, M. Marinovich, et al. 2014. Corticosteroids modulate the expression of the PKC-anchoring protein RACK-1 and cytokine release in THP-1 cells. Pharmacol. Res. 81:10–16.
20. Cullen, T., A. W. Thomas, R. Webb, and M. G. Hughes. 2015. The relationship between interleukin-6 in saliva, venous and capillary plasma, at rest and in response to exercise. Cytokine 71:397–400.
21. Dallman, M., A. Strack, S. Akana, M. Bradbury, and E. Hanson. 1993. Feast and famine: critical role of glucorticoids with insulin in daily energy flow. Front. Neuroendocrinol. 14:303–347.
22. Darwent, D., N. Lamond, and D. Dawson. 2008. The sleep and performance of train drivers during an extended freight-haul operation. Appl. Ergon. 39:614–622.
23. Derijk, R., D. Michelson, B. Karp, J. Petrides, E. Galliven, P. Deuster, et al. 1997. Exercise and circadian rhythm-induced variations in plasma cortisol differentially regulate interleukin-1 beta (IL-1 beta), IL-6, and tumor necrosis factor-alpha (TNF alpha) production in humans: high sensitivity of TNF alpha and resistance of IL-6. J. Clin. Endocrinol. Metab. 82:2182–2191.
24. Desantis, A. S., A. V. Diezroux, A. Hajat, A. E. Aiello, S. H. Golden, N. S. Jenny, et al. 2012. Associations of salivary cortisol levels with inflammatory markers: the Multi-Ethnic Study of Atherosclerosis. Psychoneuroendocrinology 37:1009–1018.
25. Elenkov, I. J. 2008. Neurohormonal-cytokine interactions: implications for inflammation, common human diseases and well-being. Neurochem. Int. 52:40–51.
26. Elenkov, I. J., and G. P. Chrousos. 1999. Stress hormones, Th1/Th2 patterns, Pro/Anti-inflammatory cytokines and susceptibility to disease. Trends Endocrinol. Metab. 10:359–368.
27. Elenkov, I. J., and G. P. Chrousos. 2002. Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann. N. Y. Acad. Sci. 966:290–303.
28. Eriksson, M., E. Sartono, C. L. Martins, C. Bale, M. L. Garly, H. Whittle, et al. 2007. A comparison of ex vivo cytokine production in venous and capillary blood. Clin. Exp. Immunol. 150:469–476.
29. Faulkner, S. H., K. L. Spilsbury, J. Harvey, A. Jackson, J. Huang, M. Platt, et al. 2014. The detection and measurement of interleukin-6 in venous and capillary blood samples, and in sweat collected at rest and during exercise. Eur. J. Appl. Physiol. 114:1207–1216.
30. Ferguson, S. A., B. Aisbett, S. M. Jay, K. Onus, C. Lord, M. Sprajcer, et al. 2011. Design of a valid simulation for researching physical, physiological and cognitive performance in volunteer firefighters during bushfire deployment. Pp. 196–204 in R. Thornton, ed. Bushfire cooperative research centre/Australasian fire and emergency service authorities council conference research forum. Bushfire Cooperative Research Centre, Sydney, New South Wales.
31. Field, A. 2009. Discovering statistics using SPSS. Sage, London.
32. Findlay, J. W., W. C. Smith, J. W. Lee, G. D. Nordblom, I. Das, B. S. Desilva, et al. 2000. Validation of immunoassays for bioanalysis: a pharmaceutical industry perspective. J. Pharm. Biomed. Anal. 21:1249–1273.
33. Finnerty, C. C., M. G. Jeschke, D. N. Herndon, R. Gamelli, N. Gibran, M. Klein, et al. 2008. Temporal cytokine profiles in severely burned patients: a comparison of adults and children. Mol. Med. 14:553–560.
34. Fisher, C. D. 2000. Mood and emotions while working: missing pieces of job satisfaction? J. Organ. Behav. 21:185–202.
35. Frank, M., Z. Miguel, L. Watkins, and S. Maier. 2010. Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide. Brain Behav. Immun. 24:19–30.
36. Gómez-González, B., E. Domínguez-Salazar, G. Hurtado-Alvarado, E. Esqueda-Leon, R. Santana-Miranda, J. A. Rojas-Zamorano, et al. 2012. Role of sleep in the regulation of the immune system and the pituitary hormones. Ann. N. Y. Acad. Sci. 1261:97–106.
37. Gundersen, Y., P. K. Opstad, T. Reistad, I. Thrane, and P. Vaagenes. 2006. 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.
38. Gunga, H. C., A. Maillet, K. Kirsch, L. Röcker, C. Gharib, and R. Vaernes. 1993. European isolation and confinement study. Water and salt turnover. Adv. Space Biol. Med. 3:185–200.
39. Haddad, J. J., N. E. Saadé, and B. Safieh-Garabedian. 2002. Cytokines and neuro-immune-endocrine interactions: a role for the hypothalamic-pituitary-adrenal revolving axis. J. Neuroimmunol. 133:1–19.
40. Hailes, W. S., D. Slivka, J. Cuddy, and B. Ruby. 2011. Human plasma inflammatory response during 5 days of exercise training in the heat. J. Therm. Biol 36:277–282.
41. Hajat, A., A. Diez-Roux, T. G. Franklin, T. Seeman, S. Shrager, N. Ranjit, et al. 2010. Socioeconomic and race/ethnic differences in daily salivary cortisol profiles: the multi-ethnic study of atherosclerosis. Psychoneuroendocrinology 35:932–943.
42. Hill, E. E., E. Zack, C. Battaglini, M. Viru, A. Viru, and A. C. Hackney. 2008. Exercise and circulating cortisol levels: the intensity threshold effect. J. Endocrinol. Invest. 31:587–591.
43. Kales, S. N., E. S. Soteriades, C. A. Christophi, and D. C. Christiani. 2007. Emergency duties and deaths from heart disease among firefighters in the United States. N. Engl. J. Med. 356:1207–1215.
44. Karlovic, D., A. Serretti, N. Vrkic, M. Martinac, and D. Marcinko. 2012. Serum concentrations of CRP, IL-6, TNF-alpha and cortisol in major depressive disorder with melancholic or atypical features. Psychiatry Res. 198:74–80.
45. Kemeny, M. E. 2007. Emotions and the immune system. Pp. 619–629 in R. Ader, ed. Psychoneuroimmunology. Academic Press, Waltham, MA.
46. Kenefick, R. W., and M. N. Sawka. 2007. Hydration at the work site. J. Am. Coll. Nutr. 26:597S–603S.
47. Kunz-Ebrecht, S. R., C. Kirschbaum, M. Marmot, and A. Steptoe. 2004. Differences in cortisol awakening response on work days and weekends in women and men from the Whitehall II cohort. Psychoneuroendocrinology 29:516–528.
48. Larsen, B., R. Snow, G. Vincent, J. Tran, A. Wolkow, and B. Aisbett. 2015. Multiple days of heat exposure on firefighters’ work performance and physiology. PLoS ONE 10:e0136413.
49. Liberati, T. A., R. A. Trammell, M. Randle, S. Barrett, and L. A. Toth. 2013. Cytokine and chemokine responses of lung exposed to surrogate viral and bacterial infections. Comp. Med. 63:114–126.
50. Lieberman, H. R., G. P. Bathalon, C. M. Falco, M. F. Kramer, C. A. Morgan, and P. Niro. 2005. Severe decrements in cognition function and mood induced by sleep loss, heat, dehydration, and undernutrition during simulated combat. Biol. Psychiatry 57:422–429.
51. Lundeland, B., Y. Gundersen, P. K. Opstad, I. Thrane, Y. Zhang, R. W. Olaussen, et al. 2012. One week of multifactorial high-stress military ranger training affects Gram-negative signalling. Scand. J. Clin. Lab. Invest. 72:547–554.
52. Lutgendorf, S. K., A. Z. Weinrib, F. Penedo, D. Russell, K. Degeest, E. S. Costanzo, et al. 2008. Interleukin-6, cortisol, and depressive symptoms in ovarian cancer patients. J. Clin. Oncol. 26:4820–4827.
53. Mackin, P., and A. H. Young. 2004. The role of cortisol and depression: exploring new opportunities for treatments. Psychiatr. Times 21:92–95.
54. Mcewen, B. S. 1998. Protective and damaging effects of stress mediators. N. Engl. J. Med. 338:171–179.
55. Mcewen, B. S., C. A. Biron, K. W. Brunson, K. Bulloch, W. H. Chambers, F. S. Dhabhar, et al. 1997. The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res. Rev. 23:79–133.
56. Miller, G. E., S. Cohen, and A. K. Ritchey. 2002. Chronic psychological stress and the regulation of pro-inflammatory cytokines: a glucocorticoid-resistance model. Health Psychol. 21:531–541.
57. Nguyen, H. P., M. Björkqvist, F. J. Bode, M. Stephan, and S. Von Hörsten. 2010. Serum levels of a subset of cytokines show high interindividual variability and are not altered in rats transgenic for Huntington′s disease. PLos Curr. 2:1–5.
58. Nicolson, N. A. 2008. Measurement of cortisol. Pp. 37–73 in L. J. Luecken and L. C. Gallo, eds. Handbook of physiological research methods in health psychology. Sage Publications Inc, Thousand Oaks, CA.
59. Nijm, J., and L. Jonasson. 2009. Inflammation and cortisol response in coronary artery disease. Ann. Med. 41:224–233.
60. Nijm, J., M. Kristenson, A. G. Olsson, and L. Jonasson. 2007. Impaired cortisol response to acute stressors in patients with coronary disease. Implications for inflammatory activity. J. Intern. Med. 262:375–384.
61. Opstad, P. K. 1994. Circadian rhythm of hormones is extinguished during prolonged physical stress, sleep and energy deficiency in young men. Eur. J. Endocrinol. 131:56–66.
62. Opstad, P. K., and A. Aakvaag. 1981. The effect of a high calory diet on hormonal changes in young men during prolonged physical strain and sleep deprivation. Eur. J. Appl. Physiol. 46:31–39.
63. Payne, R., S. Welham, and S. Harding. 2011. A guide to REML in GenStat, 16th ed. VSN International, Hempstead, Hertfordshire, U.K.
64. Petrovsky, N. 2001. Towards a unified model of neuroendocrine–immune interaction. Immunol. Cell Biol. 79:350–357.
65. Phillips, M., K. Netto, W. Payne, D. Nichols, C. Lord, N. Brooksbank, et al. 2011. Frequency, intensity and duration of physical tasks performed by Australian rural firefighters during bushfire suppression. Pp. 205–212 in R. P. Thornton, ed. Bushfire cooperative research center/Australasian fire authorities council conference research forum. Bushfire Cooperative Research Centre, Sydney, New South Wales.
66. Phillips, M., W. Payne, C. Lord, K. Netto, D. Nichols, and B. Aisbett. 2012. Identification of physically demanding tasks performed during bushfire suppression by Australian rural firefighters. Appl. Ergon. 43:435–441.
67. Phillips, M., W. R. Payne, K. Netto, S. Cramer, D. Nichols, G. K. Mcconell, et al. 2015. Oxygen uptake and heart rate during simulated wildfire suppression tasks performed by Australian rural firefighters. Occup. Med. Health Aff. 3:198. doi: 10.4172/2329-6879.1000198.
68. Piazza, J. R., S. T. Charles, R. S. Stawski, and D. M. Almeida. 2013. Age and the association between negative affective states and diurnal cortisol. Psychol. Aging 28:47–56.
69. Pledge, D., J.-F. Grosset, and G. L. Onambélé-Pearson. 2011. Is there a morning-to-evening difference in the acute IL-6 and cortisol responses to resistance exercise? Cytokine 55:318–323.
70. Pruessner, J. C., C. Kirschbaum, G. Meinlschmid, and D. H. Hellhammer. 2003. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28:916–931.
71. Raines, J., R. Snow, A. Petersen, J. Harvey, D. Nichols, and B. Aisbett. 2012. Pre-shift fluid intake: effect on physiology, work and drinking during emergency wildfire fighting. Appl. Ergon. 43:532–540.
72. Raines, J., R. Snow, A. Petersen, J. Harvey, D. Nichols, and B. Aisbett. 2013. The effect of prescribed fluid consumption on physiology and work behavior of wildfire fighters. Appl. Ergon. 44:404–413.
73. Ranjit, N., A. V. Diez-Roux, B. Sanchez, T. Seeman, S. Shea, S. Shrager, et al. 2009. Association of salivary cortisol circadian pattern with cynical hostility: multi-ethnic study of atherosclerosis. Psychosom. Med. 71:748–755.
74. Riechlin, S. 1993. Neuroendocrine-immune interactions. N. Engl. J. Med. 329:1246–1253.
75. Silverman, M. N., and E. M. Sternberg. 2012. Glucocorticoid regulation of inflammation and its functional correlates: from HPA axis to glucocorticoid receptor dysfunction. Ann. N. Y. Acad. Sci. 1261:55–63.
76. Smith, E. M., P. Cadet, G. B. Stefano, M. R. Opp, and J. T. K. Hughes. 1999. IL-10 as a mediator in the HPA axis and brain. J. Neuroimmunol. 100:140–148.
77. Spiegel, K., R. Leproult, and E. Van Cauter. 1999. Impact of sleep debt on metabolic and endocrine function. Lancet 354:1435–1439.
78. Steensberg, A., C. P. Fischer, C. Keller, K. Moller, and B. K. Pedersen. 2003. IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans. Am. J. Physiol. 285:433–437.
79. Steptoe, A., M. Hamer, and Y. Chida. 2007. The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav. Immun. 21:901–912.
80. Swiston, J. R., W. Davidson, S. Attridge, G. T. Li, M. Brauer, and S. F. V. Eeden. 2008. Wood smoke exposure induces a pulmonary and systemic inflammatory response in firefighters. European Respiratory Journal. European Respiratory Society, Sheffield, U.K.
81. Thieringer, R., C. B. Le Grand, L. Carbin, T. Q. Cai, B. Wong, S. D. Wright, et al. 2001. 11 Beta-hydroxysteroid dehydrogenase type 1 is induced in human monocytes upon differentiation to macrophages. J. Immunol. 167:30–35.
82. Turnbull, A. V., and C. L. Rivier. 1999. Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol. Rev. 79:1–71.
83. Van Dongen, H. P., E. Olofsen, D. F. Dinges, and G. Maislin. 2004. Mixed-model regression analysis and dealing with interindividual differences. Methods Enzymol. 225:117–126.
84. Vgontzas, A. N., E. O. Bixler, G. P. Chrousos, and S. Pejovic. 2008. Obesity and sleep disturbances: meaningful sub-typing of obesity. Arch. Physiol. Biochem. 114:224–236.
85. Vincent, G., S. A. Ferguson, B. Larsen, A. Wolkow, J. Tran, and B. Aisbett. 2015. Sleep restriction during simulated wildfire suppression: effect on physical task performance. PLoS ONE 10. doi: 10.1371/journal.pone.0115329.
86. Walsh, N. P., and M. Whitham. 2006. Exercising in environmental extremes: a greater threat to immune function? Sports Med. 36:941–976.
87. Weiskopf, R. B., R. Yau, R. Sanchez, C. Lowell, and P. Toy. 2009. Microarray kit analysis of cytokines in blood product units and segments. Transfusion 49:2269–2275.
88. Wolkow, A., K. Netto, P. Langridge, J. Green, D. Nichols, M. Sergeant, et al. 2014. Coronary heart disease risk in volunteer firefighters in Victoria, Australia. Arch. Environ. Occup. Health 69:112–120.
89. Wolkow, A., B. Aisbett, J. Reynolds, S. A. Ferguson, and L. C. Main. 2015a. The impact of sleep restriction while performing simulated physical firefighting work on cortisol and heart rate responses. Int. Arch. Occup. Environ. Health. doi:10.1007/s00420-015-1085-3. [Epub ahead of print]
90. Wolkow, A., S. A. Ferguson, G. E. Vincent, B. Larsen, B. Aisbett, and L. C. Main. 2015b. The impact of sleep restriction and simulated physical firefighting work on acute inflammatory stress responses. PLoS ONE 10:e0138128.
91. Woods, A. M., and A. M. Judd. 2008. Interleukin-4 increases cortisol release and decreases adrenal androgen release from bovine adrenal cells. Domest. Anim. Endocrinol. 34:372–382.
92. Zhou, X., M. S. Fragala, J. E. Mcelhaney, and G. A. Kuchel. 2010. Conceptual and methodological issues relevant to cytokine and inflammatory marker measurements in clinical research. Curr. Opin. Clin. Nutr. Metab. Care 13:541–547.