Diurnal Changes in Distribution Characteristics of Salivary Cortisol and Immunoglobulin A Concentrations
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.2. Experimental Procedures and Salivary Cortisol Measurement
2.3. Statistical Analysis
3. Results
4. Discussion
4.1. Diurnal Changes in Salivary Cortisol
4.2. Diurnal Changes in Secretory Immunoglobulin A
4.3. Log Transformation of Salivary Cortisol and Secretory Immunoglobulin A Concentrations
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Hellhammer, D.H.; Wüst, S.; Kudielka, B.M. Salivary cortisol as a biomarker in stress research. Psychoneuroendocrinology 2009, 34, 163–171. [Google Scholar] [CrossRef] [PubMed]
- Gozansky, W.S.; Lynn, J.S.; Laudenslager, M.L.; Kohrt, W.M. Salivary cortisol determined by enzyme immunoassay is preferable to serum total cortisol for assessment of dynamic hypothalamic-pituitary-adrenal axis activity. Clin. Endocrinol. (Oxf.) 2005, 63, 336–341. [Google Scholar] [CrossRef] [PubMed]
- Rydstedt, L.W.; Devereux, J.J. Psychosocial job strain and sleep quality interaction leading to insufficient recovery. Int. J. Environ. Res. Public Health 2013, 10, 5863–5873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gutteling, B.M.; de Weerth, C.; Buitelaar, J.K. Prenatal stress and children’s cortisol reaction to the first day of school. Psychoneuroendocrinology 2005, 30, 541–549. [Google Scholar] [CrossRef] [PubMed]
- Dettweiler, U.; Becker, C.; Auestad, B.H.; Simon, P.; Kirsch, P. Stress in school. Some empirical hints on the circadian cortisol rhythm of children in outdoor and indoorc classes. Int. J. Environ. Res. Public Health 2017, 14, 475. [Google Scholar] [CrossRef] [PubMed]
- Kirschbaum, C.; Hellhammer, D.H. Noise and stress-salivary cortisol as a non-invasive measure of allostatic load. Noise Health 1999, 1, 57–66. [Google Scholar] [PubMed]
- Lefèvre, M.; Carlier, M.C.; Champelovier, P.; Lambert, J.; Laumon, B.; Evrard, A.S. Effects of aircraft noise exposure on saliva cortisol near airports in France. Occup. Environ. Med. 2017, 74, 612–618. [Google Scholar] [CrossRef] [PubMed]
- MacMillan, H.L.; Georgiades, K.; Duku, E.K.; Shea, A.; Steiner, M.; Niec, A.; Tanaka, M.; Gensey, S.; Spree, S.; Vella, E.; et al. Cortisol response to stress in female youths exposed to childhood maltreatment: Results of the youth mood project. Biol. Psychiatry 2009, 66, 62–68. [Google Scholar] [CrossRef] [PubMed]
- Alink, L.R.; Cicchetti, D.; Kim, J.; Rogosch, F.A. Longitudinal associations among child maltreatment, social functioning, and cortisol regulation. Dev. Psychol. 2012, 48, 224–236. [Google Scholar] [CrossRef] [PubMed]
- Ochiai, H.; Ikei, H.; Song, C.; Kobayashi, M.; Takamatsu, A.; Kagawa, T.; Li, Q.; Kumeda, S.; Imai, M.; Miyazaki, Y. Physiological and psychological effects of a forest therapy program on middle-aged females. Int. J. Environ. Res. Public Health 2015, 12, 15222–15232. [Google Scholar] [CrossRef] [PubMed]
- Roe, J.J.; Thompson, C.W.; Aspinall, P.A.; Brewer, M.J.; Duff, E.I.; Miller, D.; Mitchell, R.; Clow, A. Green space and stress: Evidence from cortisol measures in deprived urban communities. Int. J. Environ. Res. Public Health 2013, 10, 4086–4103. [Google Scholar] [CrossRef] [PubMed]
- Haluza, D.; Schönbauer, R.; Cervinka, R. Green perspectives for public health: A narrative review on the physiological effects of experiencing outdoor nature. Int. J. Environ. Res. Public Health 2014, 11, 5445–5461. [Google Scholar] [CrossRef] [PubMed]
- Kirschbaum, C.; Hellhammer, D.H. Salivary cortisol. Encycl. Stress 2000, 3, 379–383. [Google Scholar]
- Fries, E.; Dettenborn, L.; Kirschbaum, C. The cortisol awakening response (CAR): Facts and future directions. Int. J. Psychophysiol. 2009, 72, 67–73. [Google Scholar] [CrossRef] [PubMed]
- Wüst, S.; Wolf, J.; Hellhammer, D.H.; Federenko, I.; Schommer, N.; Kirschbaum, C. The cortisol awakening response—Normal values and confounds. Noise Health 2000, 2, 79–88. [Google Scholar] [PubMed]
- Clow, A.; Hucklebridge, F.; Stalder, T.; Evans, P.; Thorn, L. The cortisol awakening response: More than a measure of HPA axis function. Neurosci. Biobehav. Rev. 2010, 35, 97–103. [Google Scholar] [CrossRef] [PubMed]
- Hek, K.; Direk, N.; Newson, R.S.; Hofman, A.; Hoogendijk, W.J.; Mulder, C.L.; Tiemeier, H. Anxiety disorders and salivary cortisol levels in older adults: A population-based study. Psychoneuroendocrinology 2013, 38, 300–305. [Google Scholar] [CrossRef] [PubMed]
- Adam, E.K.; Kumari, M. Assessing salivary cortisol in large-scale, epidemiological research. Psychoneuroendocrinology 2009, 34, 1423–1436. [Google Scholar] [CrossRef] [PubMed]
- Duramad, P.; Holland, N.T. Biomarkers of immunotoxicity for environmental and public health research. Int. J. Environ. Res. Public Health 2011, 8, 1388–1401. [Google Scholar] [CrossRef] [PubMed]
- Fagarasan, S.; Honjo, T. Intestinal IgA synthesis: Regulation of front-line body defences. Nat. Rev. Immunol. 2003, 3, 63–72. [Google Scholar] [CrossRef] [PubMed]
- Hamuro, K.; Kotani, Y.; Toba, M.; Kakumoto, K.; Kohda, N. Comparison of salivary IgA secretion rate collected by the aspiration method and swab method. Biosci. Microbiota Food Health 2013, 32, 107–112. [Google Scholar] [CrossRef] [PubMed]
- Tsujita, S.; Morimoto, K. Secretory IgA in saliva can be a useful stress marker. Environ. Health Prev. Med. 1999, 4, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Dimitriou, L.; Sharp, N.C.; Doherty, M. Circadian effects on the acute responses of salivary cortisol and IgA in well trained swimmers. Br. J. Sports Med. 2002, 36, 260–264. [Google Scholar] [CrossRef] [PubMed]
- Li, T.L.; Gleeson, M. The effect of single and repeated bouts of prolonged cycling and circadian variation on saliva flow rate, immunoglobulin A and alpha-amylase responses. J. Sports Sci. 2004, 22, 1015–1024. [Google Scholar] [CrossRef] [PubMed]
- Shirakawa, T.; Mitome, M.; Oguchi, H. Circadian rhythms of S-IgA and cortisol in whole saliva—Compensatory mechanism of oral immune system for nocturnal fall of saliva secretion—. Pediat. Dent. J. 2004, 14, 115–120. [Google Scholar] [CrossRef]
- Hucklebridge, F.; Clow, A.; Evans, P. The relationship between salivary secretory immunoglobulin A and cortisol: Neuroendocrine response to awakening and the diurnal cycle. Int. J. Psychophysiol. 1998, 31, 69–76. [Google Scholar] [CrossRef]
- Kobayashi, H.; Song, C.; Ikei, H.; Kagawa, T.; Miyazaki, Y. Analysis of individual variations in autonomic responses to urban and forest environments. Evid. Based Complement. Altern. Med. 2015, 2015, 671094. [Google Scholar] [CrossRef] [PubMed]
- Phipson, B.; Smyth, G.K. Permutation p-values should never be zero: Calculating exact p-values when permutation are randomly drawn. Stat. Appl. Genet. Mol. Biol. 2010, 9. [Google Scholar] [CrossRef] [PubMed]
- Thadewald, T.; Büning, H. Jarque–Bera test and its competitors for testing normality: A power comparison. J. Appl. Stat. 2007, 34, 87–105. [Google Scholar] [CrossRef]
- Smyth, J.; Ockenfels, M.; Gorin, A.; Catley, D.; Porter, L.S.; Kirschbaum, C.; Hellhammer, D.H.; Stone, A.A. Individual differences in the diurnal cycle of cortisol. Psychoneuroendocrinology 1997, 22, 89–105. [Google Scholar] [CrossRef]
- Kirschbaum, C.; Kudielka, B.M.; Gaab, J.; Schommer, N.C.; Hellhammer, D.H. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom. Med. 1999, 61, 154–162. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, H.; Miyazaki, Y. Distribution characteristics of salivary cortisol measurements in a healthy young male population. J. Physiol. Anthropol. 2015, 34, 30. [Google Scholar] [CrossRef] [PubMed]
- Smider, N.A.; Essex, M.J.; Kalin, N.H.; Buss, K.A.; Klein, M.H.; Davidson, R.J.; Goldsmith, H.H. Salivary cortisol as a predictor of socioemotional adjustment during kindergarten: A prospective study. Child Dev. 2002, 73, 75–92. [Google Scholar] [CrossRef] [PubMed]
- Gordis, E.B.; Granger, D.A.; Susman, E.J.; Trickett, P.K. Salivary alpha amylase–cortisol asymmetry in maltreated youth. Horm. Behav. 2008, 53, 96–103. [Google Scholar] [CrossRef] [PubMed]
- Cohen, N.; Flamenbaum, W. Obesity and hypertension. Demonstration of a “floor effect.”. Am. J. Med. 1986, 80, 177–181. [Google Scholar] [PubMed]
- Hansen, Å.M.; Garde, A.H.; Christensen, J.M.; Eller, N.H.; Netterstrøm, B. Evaluation of a radioimmunoassay and establishment of a reference interval for salivary cortisol in healthy subjects in Denmark. Scand. J. Clin. Lab. Investig. 2003, 63, 303–310. [Google Scholar] [CrossRef]
- Beil, K.; Hanes, D. The influence of urban natural and built environments on physiological and psychological measures of stress—A pilot study. Int. J. Environ. Res. Public Health 2013, 10, 1250–1267. [Google Scholar] [CrossRef] [PubMed]
- Turner-Cobb, J.M.; Sephton, S.E.; Koopman, C.; Blake-Mortimer, J.; Spiegel, D. Social support and salivary cortisol in women with metastatic breast cancer. Psychosom. Med. 2000, 62, 337–345. [Google Scholar] [CrossRef] [PubMed]
- Sephton, S.E.; Sapolsky, R.M.; Kraemer, H.C.; Spiegel, D. Diurnal cortisol rhythm as a predictor of breast cancer survival. J. Natl. Cancer Inst. 2000, 92, 994–1000. [Google Scholar] [CrossRef] [PubMed]
- Yehuda, R.; Golier, J.A.; Kaufman, S. Circadian rhythm of salivary cortisol in Holocaust survivors with and without PTSD. Am. J. Psychiatry. 2005, 162, 998–1000. [Google Scholar] [CrossRef] [PubMed]
- Phillips, A.C.; Carroll, D.; Evans, P.; Bosch, J.A.; Clow, A.; Hucklebridge, F.; Der, G. Stressful life events are associated with low secretion rates of immunoglobulin A in saliva in the middle aged and elderly. Brain Behav. Immun. 2006, 20, 191–197. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moreira, A.; Mortatti, A.L.; Arruda, A.F.; Freitas, C.G.; de Arruda, M.; Aoki, M.S. Salivary IgA response and upper respiratory tract infection symptoms during a 21-week competitive season in young soccer players. J. Strength Cond. Res. 2014, 28, 467–473. [Google Scholar] [CrossRef] [PubMed]
- Laurent, H.K.; Stroud, L.R.; Brush, B.; D’Angelo, C.; Granger, D.A. Secretory IgA reactivity to social threat in youth: Relations with HPA, ANS, and behavior. Psychoneuroendocrinology 2015, 59, 81–90. [Google Scholar] [CrossRef] [PubMed]
Variable | Age (Years) | Height (cm) | Weight (kg) |
---|---|---|---|
Mean | 22.3 | 172.0 | 65.6 |
SD * | 1.6 | 5.7 | 10.2 |
Max | 29 | 187.5 | 110.0 |
Min | 20 | 155.0 | 50.0 |
Variable | Cortisol (nmol/L) | S-IgA (mg/L) | ||||
---|---|---|---|---|---|---|
Morning | Afternoon | p | Morning | Afternoon | p | |
Mean | 19.97 | 8.84 | <0.01 ** | 245.0 | 211.3 | 0.08 |
Median | 18.76 | 8.28 | <0.01 ** | 204.0 | 189.1 | 0.50 |
SD | 7.17 | 3.12 | <0.01 ** | 163.7 | 119.4 | 0.03 * |
CV | 35.9% | 35.3% | 0.90 | 66.8% | 56.5% | 0.17 |
Q1 | 15.17 | 6.62 | <0.01 ** | 123.5 | 123.7 | 0.94 |
Q3 | 24.00 | 10.48 | <0.01 ** | 349.4 | 265.7 | 0.02 * |
IQR | 8.83 | 3.86 | 0.01 * | 225.9 | 142.0 | 0.01 * |
Skewness | 0.49 | 1.06 | 0.02 * | 1.34 | 1.12 | 0.80 |
Kurtosis | 2.80 | 4.78 | <0.01 ** | 5.46 | 4.12 | 0.80 |
JB | 4.7 | 36.1 | 62.3 | 29.5 | ||
p = 0.10 | p < 0.01 ** | p < 0.01 ** | p < 0.01 ** |
Variable | Cortisol (ln(nmol/L)) | S-IgA (ln(mg/L)) | ||||
---|---|---|---|---|---|---|
Morning | Afternoon | p | Morning | Afternoon | p | |
Mean | 2.93 | 2.12 | <0.01 ** | 5.26 | 5.18 | 0.44 |
Median | 2.93 | 2.11 | <0.01 ** | 5.32 | 5.24 | 0.50 |
SD | 0.38 | 0.34 | 0.29 | 0.78 | 0.66 | 0.42 |
CV | 13.0% | 16.1% | 0.06 | 14.9% | 12.85% | 0.48 |
Skewness | −0.51 | 0.10 | <0.01 ** | −1.15 | −1.84 | 0.61 |
Kurtosis | 3.40 | 2.66 | <0.01 ** | 6.01 | 12.57 | 0.09 |
JB | 5.7 | 0.7 | 67.6 | 495.0 | ||
p = 0.06 | p = 0.70 | p < 0.01 ** | p < 0.01 ** |
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Kobayashi, H.; Song, C.; Ikei, H.; Park, B.-J.; Kagawa, T.; Miyazaki, Y. Diurnal Changes in Distribution Characteristics of Salivary Cortisol and Immunoglobulin A Concentrations. Int. J. Environ. Res. Public Health 2017, 14, 987. https://doi.org/10.3390/ijerph14090987
Kobayashi H, Song C, Ikei H, Park B-J, Kagawa T, Miyazaki Y. Diurnal Changes in Distribution Characteristics of Salivary Cortisol and Immunoglobulin A Concentrations. International Journal of Environmental Research and Public Health. 2017; 14(9):987. https://doi.org/10.3390/ijerph14090987
Chicago/Turabian StyleKobayashi, Hiromitsu, Chorong Song, Harumi Ikei, Bum-Jin Park, Takahide Kagawa, and Yoshifumi Miyazaki. 2017. "Diurnal Changes in Distribution Characteristics of Salivary Cortisol and Immunoglobulin A Concentrations" International Journal of Environmental Research and Public Health 14, no. 9: 987. https://doi.org/10.3390/ijerph14090987