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International Journal of Biometeorology

, Volume 62, Issue 2, pp 165–175 | Cite as

Weather conditions: a neglected factor in human salivary cortisol research?

  • Goran Milas
  • Daniela Šupe-Domić
  • Irena Drmić-Hofman
  • Lada Rumora
  • Irena Martinović Klarić
Original Paper

Abstract

There is ample evidence that environmental stressors such as extreme weather conditions affect animal behavior and that this process is in part mediated through the elevated activity of the hypothalamic pituitary adrenal axis which results in an increase in cortisol secretion. This relationship has not been extensively researched in humans, and weather conditions have not been analyzed as a potential confounder in human studies of stress. Consequently, the goal of this paper was to assess the relationship between salivary cortisol and weather conditions in the course of everyday life and to test a possible moderating effect of two weather-related variables, the climate region and timing of exposure to outdoors conditions. The sample consisted of 903 secondary school students aged 18 to 21 years from Mediterranean and Continental regions. Cortisol from saliva was sampled in naturalistic settings at three time points over the course of a single day. We found that weather conditions are related to salivary cortisol concentration and that this relationship may be moderated by both the specific climate and the anticipation of immediate exposure to outdoors conditions. Unpleasant weather conditions are predictive for the level of salivary cortisol, but only among individuals who anticipate being exposed to it in the immediate future (e.g., in students attending school in the morning shift). We also demonstrated that isolated weather conditions or their patterns may be relevant in one climate area (e.g., Continental) while less relevant in the other (e.g., Mediterranean). Results of this study draw attention to the importance of controlling weather conditions in human salivary cortisol research.

Keywords

Salivary cortisol HPA axis activity Weather conditions Climate Naturalistic study 

Notes

Acknowledgements

This study (CLASS) was taken with the framework of the project “Modernity Stress, Youth and Modernization” (09.01/408) financed by the Croatian Science Foundation, awarded to Dr. Irena Martinović Klarić. We are thankful to the Croatian Meteorological and Hydrological Service for providing meteorological data and especially to Mrs. Dubravka Rasol and Mr. Damir Mlinek for their kind assistance. We sincerely thank to Dr. Natasha Levak for proofreading of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adam EK, Kumari M (2009) Assessing salivary cortisol in large-scale, epidemiological research. Psychoneuroendocrino 34:1423–1436CrossRefGoogle Scholar
  2. Agrimonti F, Angeli A, Frairia R, Fazzari A, Tamagnone C, Fornaro D et al (1982) Circannual rhythmicities of cortisol levels in the peripheral plasma of healthy subjects. Chronobiologia 9:107–114Google Scholar
  3. Aiken LS, West SG (1991) Multiple regression: testing and interpreting interactions. Sage, Thousand OaksGoogle Scholar
  4. Arsenault-Lapierre G, Chertkow H, Lupien S (2010) Seasonal effects on cortisol secretion in normal aging, mild cognitive impairment and Alzheimer’s disease. Neurobiol Aging 31:1051–1054CrossRefGoogle Scholar
  5. Baron M, Kenny A (1986) The moderator–mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol 51:1174–1182CrossRefGoogle Scholar
  6. Bellastella A, Criscuolo T, Mango A, Perrone L, Sinisi AA, Faggiano M (1983) Circannual rhythms of plasma luteinizing hormone, follicle-stimulating hormone, testosterone, prolactin and cortisol in prepuberty. Clin Endocrinol 19:453–459CrossRefGoogle Scholar
  7. Belmaker RH, Agam G (2008) Major depressive disorder. N Engl J Med 358:55–68CrossRefGoogle Scholar
  8. Bennett J (2000) Focus on research methods mediator and moderator variables in nursing research: conceptual and statistical differences. Res Nurs Health 23:415–420CrossRefGoogle Scholar
  9. Boesch M, Sefidan S, Annen H, Ehlert U, Roos L, Van Uum S et al (2015) Hair cortisol concentration is unaffected by basic military training, but related to sociodemographic and environmental factors. Stress 18:35–41CrossRefGoogle Scholar
  10. Brunner EJ, Hemingway H, Walker BR, Page M, Clarke P, Juneja M et al (2002) Adrenocortical, autonomic, and inflammatory causes of the metabolic syndrome. Circulation 106:2659–2665CrossRefGoogle Scholar
  11. Brzović N, Strelec Mahović N (1999) Cyclonic activity and severe Jugo in the Adriatic. Phys Chem Earth 24:653–657CrossRefGoogle Scholar
  12. Buss DM (2008) Evolutionary psychology: the new science of the mind. Pearson, BostonGoogle Scholar
  13. Chrousos GP (2009) Stress and disorders of the stress system. Nat Rev Endocrinol 5:374–381CrossRefGoogle Scholar
  14. Clow A, Thorn L, Evans P, Hucklebridge F (2004) The awakening cortisol response: methodological issues and significance. Stress 7:29–37CrossRefGoogle Scholar
  15. Connolly M (2013) Some like it mild and not too wet: the influence of weather on subjective well-being. J Happiness Stud 14:457–473CrossRefGoogle Scholar
  16. Cook TD, Campbell DT (1979) Quasi-experimentation: design and analysis issues for field settings. Houghton Mifflin Company, BostonGoogle Scholar
  17. Cunningham MR (1979) Weather, mood, and helping behavior: quasi experiments with the sunshine Samaritan. J Pers Soc Psychol 37:1974–1956Google Scholar
  18. Del Ponte A, Guagnano MT, Sensi S (1984) Time-related behaviour of endocrine secretion: circannual variations of FT3, cortisol, HGH and serum basal insulin in healthy subjects. Chronobiol Int 1:297–300CrossRefGoogle Scholar
  19. Denissen JJA, Butalid L, Penke L, van Aken MAG (2008) The effects of weather on daily mood: a multilevel approach. Emotion 8:662–667CrossRefGoogle Scholar
  20. Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130:355–391CrossRefGoogle Scholar
  21. Doane LD, Mineka S, Zinbarg RE, Craske M, Griffith JW, Adam EK (2013) Are flatter diurnal cortisol rhythms associated with major depression and anxiety disorders in late adolescence? The role of life stress and daily negative emotion. Dev Psychopathol 25:629–642CrossRefGoogle Scholar
  22. Edwards S, Clow A, Evans P, Hucklebridge F (2001) Exploration of the awakening cortisol response in relation to diurnal cortisol secretory activity. Life Sci 68:2093–2103CrossRefGoogle Scholar
  23. Fries E, Dettenborn L, Kirschbaum C (2009) The cortisol awakening response CAR: facts and future directions. Int J Psychophysiol 72:67–73CrossRefGoogle Scholar
  24. Garcia A, Marti O, Valles A, Dal-Zotto S, Armario A (2000) Recovery of the hypothalamic–pituitary–adrenal response to stress effect of stress intensity, stress duration and previous stress exposure. Neuroendocrinology 72:114–125CrossRefGoogle Scholar
  25. Gesquiere LR, Khan M, Shek L, Wango TL, Wango EO, Alberts SC et al (2008). Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus). Horm Behav 54:410–416Google Scholar
  26. Gunnar M, Vazquez DM (2001) Low cortisol and a flattening of the expected daytime rhythm: potential indices of risk in human development. Dev Psychopathol 13:515–538CrossRefGoogle Scholar
  27. Hair JF, Black WC, Babin BJ, Anderson RE (2009) Multivariate data analysis. Prentice Hall, Upper Saddle RiverGoogle Scholar
  28. Hansen AM, Garde AH, Skovgaard LT, Christensen JM (2001) Seasonal and biological variation of urinary epinephrine, norepinephrine, and cortisol in healthy women. Clin Chim Acta 309:25–35CrossRefGoogle Scholar
  29. Hansen AM, Persson R, Garde AH, Karlson B, Orbaek P (2006) Diurnal profiles of salivary cortisol on workdays among construction workers versus white-collar workers. Scand J Work Environ Health Suppl 2:22–26Google Scholar
  30. Herbert J, Goodyer IM, Grossman AB, Hastings MH, de Kloet ER, Lightman SL et al (2006) Do corticosteroids damage the brain? J Neuroendocrinol 18:393–411CrossRefGoogle Scholar
  31. Jonsdottir I, Halford C, Eek F (2012) Mental health and salivary cortisol In: Kristenson M, Garvin P, Lundberg U (eds) The role of saliva cortisol measurements in health and disease. Bentham E Books, pp 129–166. https://ebooks.benthamscience.com/book/9781608053421/
  32. Kanikowska D, Sugenoya J, Sato M, Shimizu Y, Inukai Y, Nishimura N et al (2009) Seasonal variation in blood concentrations of interleukin-6, adrenocorticotrophic hormone, metabolites of catecholamine and cortisol in healthy volunteers. Int J Biometeorol 53:479–485CrossRefGoogle Scholar
  33. Keller MC, Fredrickson BL, Ybarra O, Côté S, Johnson K, Mikels J et al (2005) A warm heart and a clear head: the contingent effects of weather on mood and cognition. Psychol Sci 16:724–731CrossRefGoogle Scholar
  34. King JA, Rosal MC, Ma YS, Reed G, Kelly TA, Stanek EJ et al (2000) Sequence and seasonal effects of salivary cortisol. Behav Med 26:67–73CrossRefGoogle Scholar
  35. Kirschbaum C, Hellhammer DH (1989) Salivary cortisol in psychobiological research: an overview. Neuropsychobiology 22:150–169CrossRefGoogle Scholar
  36. Kirschbaum C, Hellhammer DH (1994) Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrino 19:313–333CrossRefGoogle Scholar
  37. Kirschbaum C, Pirke KM, Hellhammer DH (1993) The ‘Trier Social Stress Test’—a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28:76–81CrossRefGoogle Scholar
  38. Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM et al (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav R 35:1291–1301CrossRefGoogle Scholar
  39. Matchock RL, Dorn LD, Susman EJ (2007) Diurnal and seasonal cortisol, testosterone, and DHEA rhythms in boys and girls during puberty. Chronobiol Int 24:969–990CrossRefGoogle Scholar
  40. McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873–904CrossRefGoogle Scholar
  41. McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behavi 43:2–15CrossRefGoogle Scholar
  42. McRae AL, Saladin ME, Brady KT, Upadhyaya H, Back SE, Timmerman MA (2006) Stress reactivity: biological and subjective responses to the cold pressor and trier social stressors. Hum Psychopharm Clin 21:377–385CrossRefGoogle Scholar
  43. Persson R, Garde AH, Hansen AM, Osterberg K, Larsson B, Orbaek P et al (2008) Seasonal variation in human salivary cortisol concentration. Chronobiol Int 25:923–937CrossRefGoogle Scholar
  44. Phillips DIW, Barker DJP, Fall CHD, Seckl JR, Whorwood CB, Wood PJ et al (1998) Elevated plasma cortisol concentrations: a link between low birth weight and insulin resistance syndrome? J Clin Endocrinol Metab 83:757–760Google Scholar
  45. Pruessner JC, Gaab J, Hellhammer DH, Lintz D, Schommer N, Kirschbaum C (1997) Increasing correlations between personality traits and cortisol stress responses obtained by data aggregation. Psychoneuroendocrino 22:615–625CrossRefGoogle Scholar
  46. Pruessner JC, Kirschbaum C, Meinlschmid G, Hellhammer DH (2003) Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrino 28:916–931CrossRefGoogle Scholar
  47. Reinberg A, Lagoguey M, Cesselin F, Touitou Y, Legrand JC, Delassalle A et al (1978) Circadian and circannual rhythms in plasma hormones and other variables of five healthy young human males. Acta Endocrinol 88:417–427Google Scholar
  48. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24CrossRefGoogle Scholar
  49. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255CrossRefGoogle Scholar
  50. Romero LM, Reed JM, Wingfield JC (2000) Effects of weather on corticosterone responses in wild free-living passerine birds. Gen Comp Endocrinol 118:113–122CrossRefGoogle Scholar
  51. Smith GD, Ben-Shlomo Y, Beswick A, Yarnell J, Lightman S, Elwood P (2005) Cortisol, testosterone, and coronary heart disease: prospective evidence from the Caerphilly study. Circulation 112:332–340CrossRefGoogle Scholar
  52. Sterling P, Eyer J (1988) Allostasis: a new paradigm to explain arousal pathology. In: Fisher S, Reason J (eds) Handbook of life stress, cognition and health. Wiley, New York, pp 629–649Google Scholar
  53. Šupe-Domić D, Milas G, Drmić-Hofman I, Rumora L, Martinović Klarić I (2016) Daily salivary cortisol profile: insights from the Croatian Late Adolescence Stress Study (CLASS). Biochem Med 26:408–420Google Scholar
  54. Walker BR, Best R, Noon JP, Watt GCM, Webb DJ (1997) Seasonal variation in glucocorticoid activity in healthy men. J Clin Endocrinol Metab 82:4015–4019Google Scholar
  55. Wehr TA (2001) Photoperiodism in humans and other primates: evidence and implications. J Biol Rhythm 16:348–364CrossRefGoogle Scholar
  56. Wingfield JC, Kitaysky AS (2002) Endocrine responses to unpredictable environmental events: stress or anti- stress hormones? Int Comp Biol 42:600–609CrossRefGoogle Scholar
  57. Wu A, Zumbo B (2008) Understanding and using mediators and moderators. Soc Indic Res 87:367–392CrossRefGoogle Scholar
  58. Wüst S, Federenko I, Hellhammer DH, Kirschbaum C (2000) Genetic factors, perceived chronic stress, and the free cortisol response to awakening. Psychoneuroendocrino 25:707–720CrossRefGoogle Scholar

Copyright information

© ISB 2017

Authors and Affiliations

  • Goran Milas
    • 1
  • Daniela Šupe-Domić
    • 2
  • Irena Drmić-Hofman
    • 3
    • 4
  • Lada Rumora
    • 5
  • Irena Martinović Klarić
    • 6
  1. 1.Centre for Research on Interindividual DifferencesInstitute of Social Sciences “Ivo Pilar”ZagrebCroatia
  2. 2.Department of Medical Laboratory DiagnosticsUniversity Hospital Centre SplitSplitCroatia
  3. 3.Department of Pathology, Forensic Medicine and CytologyUniversity Hospital Centre SplitSplitCroatia
  4. 4.Department of Medical Chemistry and BiochemistryUniversity of Split School of MedicineSplitCroatia
  5. 5.Department of Medical Biochemistry and Hematology, Faculty of Pharmacy and BiochemistryUniversity of ZagrebZagrebCroatia
  6. 6.Centre for Research in Social Inequalities and SustainabilityInstitute for Social Research in ZagrebZagrebCroatia

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