Journal of Behavioral Medicine

, Volume 30, Issue 1, pp 45–58 | Cite as

Associations among Salivary Cortisol, Melatonin, Catecholamines, Sleep Quality and Stress in Women with Breast Cancer and Healthy Controls

  • Linda E. Carlson
  • Tavis S. Campbell
  • Sheila N. Garland
  • Paul Grossman
Article

Dysregulations in several biological systems in breast cancer patients have been reported, including abnormalities in endocrine and sympathetic nervous system indices, as well as psychological disturbances and sleep disorders. The purpose of this exploratory study was to compare women with breast cancer to healthy control women on measures of salivary cortisol, urinary catecholamines, overnight urinary melatonin, and self-reported sleep quality, symptoms of stress, depression, anxiety and mood disturbance, to determine if discernable patterns of dysregulations across systems were apparent. Thirty-three women were tested in each group, with an average age of approximately 52 years, primarily Caucasian and well-educated. Forty percent of the women with breast cancer had stage 2 disease and they were an average of 1.36 years post-diagnosis. Women with breast cancer had significantly higher levels of disturbance on all the psychological indices, but there were no differences between groups on any of the biological measures, with the exception that the control women had higher dopamine values than the participants with breast cancer. None of the psychological scores were correlated with the biological measures. These results are consistent with other studies of early-stage breast cancer and highlight the importance of considering disease characteristics when investigating endocrine and sympathetic nervous system functioning.

KEY WORDS

breast cancer cortisol melatonin catecholamines stress depression anxiety 

REFERENCES

  1. Abercrombie, H. C., Giese-Davis, J., Sephton, S., Epel, E. S., Turner-Cobb, J. M., and Spiegel, D. (2004). Flattened cortisol rhythms in metastatic breast cancer patients. psychoneuroendocrinology 29: 1082–1092.PubMedCrossRefGoogle Scholar
  2. Andersen, B. L., Kiecolt-Glaser, J. K., and Glaser, R. (1994). A biobehavioral model of cancer stress and disease course. Am. Psychol. 49: 389–404.PubMedCrossRefGoogle Scholar
  3. Antoni, M. H. (2003). Psychoneuroendocrinology and psychoneuroimmunology of cancer: Plausible mechanisms worth pursuing? Brain Behav. Immun. 17(1): S84–S91.PubMedCrossRefGoogle Scholar
  4. Bettermann, H., Kroz, M., Girke, M., and Heckmann, C. (2001). Heart rate dynamics and cardiorespiratory coordination in diabetic and breast cancer patients. Clin. Physiol. 21: 411–420.PubMedCrossRefGoogle Scholar
  5. Bovbjerg, D. H. (2003). Circadian disruption and cancer: sleep and immune regulation. Brain Behav. Immun. 17(1): S48–S50.PubMedCrossRefGoogle Scholar
  6. Bower, J. E., Ganz, P. A., Aziz, N., and Fahey, J. L. (2002). Fatigue and proinflammatory cytokine activity in breast cancer survivors. Psychosom. Med 64: 604–611.PubMedGoogle Scholar
  7. Bower, J. E., Ganz, P. A., Dickerson, S. S., Petersen, L., Aziz, N., and Fahey, J. L. (2005). Diurnal cortisol rhythm and fatigue in breast cancer survivors. Psychoneuroendocrinology 30: 92–100.PubMedCrossRefGoogle Scholar
  8. Bubenik, G. A., Blask, D. E., Brown, G. M., Maestroni, G. J., Pang, S. F., Reiter, R. J., et al. (1998). Prospects of the clinical utilization of melatonin. Biol. Signals Recep. 7: 195–219.CrossRefGoogle Scholar
  9. Buysse, D. J., Reynolds, C. F., Monk, T. H., and Berman, S. R. (1989). The Pittsburgh Sleep Quality Index: A new instrument for psychiatric practice and research. Psychiatr. Res. 28: 193–213.CrossRefGoogle Scholar
  10. Carlson, L. E., and Garland, S. N. (2005). Impact of mindfulness-based stress reduction (MBSR) on sleep, mood, stress and fatigue symptoms in cancer outpatients. Int. J. Behav. Med. 12: 278–285.PubMedCrossRefGoogle Scholar
  11. Carlson, L. E., Speca, M., Patel, K. D., and Goodey, E. (2003). Mindfulness-based stress reduction in relations to quality of life, mood, symptoms and stress and immune parameters in breast and prostate cancer outpatients. Psychosom. Med. 65: 571–581.PubMedCrossRefGoogle Scholar
  12. Carlson, L. E., Speca, M., Patel, K. D., and Goodey, E. (2004). Mindfulness-based stress reduction in relation to quality of life, mood, symptoms of stress and levels of cortisol, dehydroepiandrosterone-Sulftate (DHEAS) and melatonin in breast and prostate cancer outpatients. Psychoneuroendocrinology 29: 448–474.PubMedCrossRefGoogle Scholar
  13. Carpenter, J. S., and Andrykowski, M. A. (1998). Psychometric evaluation of the Pittsburgh Sleep Quality Index. J. Psychosom. Res 45: 5–13.PubMedCrossRefGoogle Scholar
  14. Cassileth, B. R., Lusk, E. J., Strouse, T. B., Miller, D. S., Brown, L. L., and Cross, P. A. (1985). A psychological analysis of cancer patients and their next-of-kin. Cancer 55: 72–76.PubMedCrossRefGoogle Scholar
  15. Chambers, M. J., and Kim, J. Y. (1993). The role of state-trait anxiety in insomnia and daytime restedness. Behav. Med. 19: 42–46.PubMedCrossRefGoogle Scholar
  16. Claghorn, J. L., Mathew, R. J., Weinman, M. L., and Hruska, N. (1981). Daytime sleepiness in depression. J. Clin. Psychiatr. 42: 342–343.Google Scholar
  17. Cohen, S., and Williamson, G. M. (1991). Stress and infectious diseases in humans. Psychol. Bull. 109: 5–24.PubMedCrossRefGoogle Scholar
  18. Cowan, M. J., Graham, K. Y., and Cochrane, B. L. (1992). Comparison of a theory of quality of life between myocardial infarction and malignant melanoma: a pilot study. Progr. Cardiovasc. Nurs. 7: 18–28.Google Scholar
  19. Davidson, R., and MacKinnon, J. G. (1993). Estimation and Inference in Econometrics. Oxford University Press Oxford, England.Google Scholar
  20. Davis, S., Mirick, D. K., and Stevens, R. G. (2001). Night shift work, light at night, and risk of breast cancer. J. Nati. Cancer Inst. 93: 1557–1562.CrossRefGoogle Scholar
  21. Drafta, D. S., Stroe, E., Schindler, E. E., Teodosiu, T., Gozariu, L., and Drafta, D. (1981). Adrenal function in early and metastatic breast cancer: dexamethasone suppression of plasma cortisol. Endocrinologie 19: 115–121.PubMedGoogle Scholar
  22. Edwards, S., Hucklebridge, F., Clow, A., and Evans, P. (2003). Components of the diurnal cortisol cycle in relation to upper respiratory symptoms and perceived stress. Psychosom. Med. 65: 320–327.PubMedCrossRefGoogle Scholar
  23. Geoffriau, M., Brun, J., Chazot, G., and Claustrat, B. (1998). The physiology and pharmacology of melatonin in humans. Horm. Res. 49: 136–141.PubMedCrossRefGoogle Scholar
  24. Gold, S. M., Zakowski, S. G., Valdimarsdottir, H. B., and Bovbjerg, D. H. (2003). Stronger endocrine responses after brief psychological stress in women at familial risk of breast cancer. Psychoneuroendocrinology 28: 584–593.PubMedCrossRefGoogle Scholar
  25. Hall, M., Buysse, D. J., Nowell, P. D., Nofzinger, E. A., Houck, P., Reynolds, C. F., III, et al. (2000). Symptoms of stress and depression as correlates of sleep in primary insomnia. Psychosom. Med. 62: 227–230.PubMedGoogle Scholar
  26. Hays, J. H., and O’Brian, J. T. (1989). Endocrine and metabolic function in patients with neoplastic disease. In Herberman, R. B. (Ed.), Influence of the Host on Tumor Development (pp. 530–543). Kluwer Academic Publishers, Dordrecht.Google Scholar
  27. Hewitt, M., Rowland, J. H., and Yancik, R. (2003). Cancer survivors in the United States: age, health, and disability. J. Gerontol. A Biol. Sci. Med. Sci. 58: 82–91.PubMedGoogle Scholar
  28. Hossain, J. L., and Shapiro, C. M. (2002). The prevalence, cost implications, and management of sleep disorders: an overview. Sleep Breath. 6: 85–102.PubMedCrossRefGoogle Scholar
  29. James, G. D., Berge-Landry, H. H., Valdimarsdottir, H. B., Montgomery, G. H., and Bovbjerg, D. H. (2004). Urinary catecholamine levels in daily life are elevated in women at familial risk of breast cancer. Psychoneuroendocrinology 29: 831–838.PubMedCrossRefGoogle Scholar
  30. James, G. D., Sealey, J. E., Alderman, M., Ljungman, S., Mueller, F. B., Pecker, M. S., et al. (1988). A longitudinal study of urinary creatinine and creatinine clearance in normal subjects. Race, sex, and age differences. Am. J. Hypertens 1: 124–131.PubMedGoogle Scholar
  31. Kajimura, N., Kato, M., Sekimoto, M., Watanabe, T., Takahashi, K., Okuma, T., et al. (1998). A polysomnographic study of sleep patterns in normal humans with low- or high-anxiety personality traits. Psychiatr. Clin. Neurosci. 52: 317–320.CrossRefGoogle Scholar
  32. Kirschbaum, C., and Hellhammer, D. H. (1994). Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19: 313–333.PubMedCrossRefGoogle Scholar
  33. Koopman, C., Nouriani, B., Erickson, V., Anupindi, R., Butler, L. D., Bachmann, M. H., et al. (2002). Sleep disturbances in women with metastatic breast cancer. Breast J. 8: 362–370.PubMedCrossRefGoogle Scholar
  34. Kripke, D. F., Garfinkel, L., Wingard, D. L., Klauber, M. R., and Marler, M. R. (2002). Mortality associated with sleep duration and insomnia. Archives Gen. Psychiatr. 59: 131–136.CrossRefGoogle Scholar
  35. Kushida, C. A., Nichols, D. A., Simon, R. D., Young, T., Grauke, J. H., Britzmann, J. B., et al. (2000). Symptom-Based Prevalence of Sleep Disorders in an Adult Primary Care Population. Sleep Breath. 4: 9–14.PubMedCrossRefGoogle Scholar
  36. Leckie, M. S., and Thompson, E. (1979). Symptoms of Stress Inventory. University of Washington. Ref Type: Serial (Book,Monograph), Seattle, WA.Google Scholar
  37. Linsell, C. R., Lightman, S. L., Mullen, P. E., Brown, M. J., and Causon, R. C. (1985). Circadian rhythms of epinephrine and norepinephrine in man. J. Clin. Endocrinol. Metab 60: 1210–1215.PubMedCrossRefGoogle Scholar
  38. Lissoni, P., Barni, S., Mandala, M., Ardizzoia, A., Paolorossi, F., Vaghi, M., et al. (1999a). Decreased toxicity and increased efficacy of cancer chemotherapy using the pineal hormone melatonin in metastatic solid tumour patients with poor clinical status. Eur. J. Cancer 35: 1688–1692.PubMedCrossRefGoogle Scholar
  39. Lissoni, P., Cazzaniga, M., Tancini, G., Scardino, E., Musci, R., Barni, S., et al. (1997). Reversal of clinical resistance to LHRH analogue in metastatic prostate cancer by the pineal hormone melatonin: Efficacy of LHRH analogue plus melatonin in patients progressing on LHRH analogue alone. Eur. Urology 31: 178–181.Google Scholar
  40. Lissoni, P., Tancini, G., Paolorossi, F., Mandala, M., Ardizzoia, A., Malugani, F., et al. (1999b). Chemoneuroendocrine therapy of metastatic breast cancer with persistent thrombocytopenia with weekly low-dose epirubicin plus melatonin: a phase II study. J Pineal Res. 26: 169–173.PubMedCrossRefGoogle Scholar
  41. Lutgendorf, S. K., and Costanzo, E. S. (2003). Psychoneuroimmunology and health psychology: an integrative model. Brain Behav. Immun. 17: 225–232.PubMedCrossRefGoogle Scholar
  42. Marshall, G. D., Jr., Agarwal, S. K., Lloyd, C., Cohen, L., Henninger, E. M., and Morris, G. J. (1998). Cytokine dysregulation associated with exam stress in healthy medical students. Brain Behav. Immun. 12: 297–307.PubMedCrossRefGoogle Scholar
  43. McNair, D. A., Lorr, M., and Droppelman, L. F. (1971). Profile of Mood States . Educational and Industrial Testing Service, San Diego.Google Scholar
  44. Mormont, M. C., and Levi, F. (1997). Circadian-system alterations during cancer processes: a review. Int J Cancer, 70 : 241–247.PubMedCrossRefGoogle Scholar
  45. Pollack, L. A., Greer, G. E., Rowland, J. H., Miller, A., Doneski, D., Coughlin, S. S., et al. (2005). Cancer survivorship: a new challenge in comprehensive cancer control. Cancer Causes Control 16(1): 51–59.PubMedCrossRefGoogle Scholar
  46. Porter, L. S., Mishel, M., Neelon, V., Belyea, M., Pisano, E., and Soo, M. S. (2003). Cortisol levels and responses to mammography screening in breast cancer survivors: a pilot study. Psychosom. Med. 65: 842–848.PubMedCrossRefGoogle Scholar
  47. Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., and Hellhammer, D. H. (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.PubMedCrossRefGoogle Scholar
  48. Radloff, L. S. (1977). The CES-D Scale: A self-report depression scale for research in the general population. Appl. Psychol. Measurement 1: 385–401.Google Scholar
  49. Saez, M. C., Barriga, C., Garcia, J. J., Rodriguez, A. B., Masot, J., Duran, E., et al. (2005). Melatonin increases the survival time of animals with untreated mammary tumours: neuroendocrine stabilization. Mol. Cell Biochem. 278: 15–20.PubMedCrossRefGoogle Scholar
  50. Savard, J., and Morin, C. M. (2001). Insomnia in the context of cancer: a review of a neglected problem. J. Clin. Oncol. 19: 895–908.PubMedGoogle Scholar
  51. Savard, J., Simard, S., Blanchet, J., Ivers, H., and Morin, C. M. (2001). Prevalence, clinical characteristics, and risk factors for insomnia in the context of breast cancer. Sleep 24: 583–590.PubMedGoogle Scholar
  52. Schernhammer, E. S., Laden, F., Speizer, F. E., Willett, W. C., Hunter, D. J., Kawachi, I., et al. (2001). Rotating night shifts and risk of breast cancer in women participating in the nurses’ health study. J. Nati. Cancer Institute 93: 1563–1568.Google Scholar
  53. Sephton, S., and Spiegel, D. (2003). Circadian disruption in cancer: a neuroendocrine-immune pathway from stress to disease? Brain Behav. Immun. 17: 321–328.PubMedCrossRefGoogle Scholar
  54. Sephton, S. E., Sapolsky, R. M., Kraemer, H. C., and Spiegel, D. (2000). Diurnal cortisol rhythm as a predictor of breast cancer survival. J. Nati. Cancer Inst. 92: 944–1000.Google Scholar
  55. Shapiro, S. L., Bootzin, R. R., Figueredo, A. J., Lopez, A. M., and Schwartz, G. E. (2003). The efficacy of mindfulness-based stress reduction in the treatment of sleep disturbance in women with breast cancer: an exploratory study. J. Psychosom. Res. 54: 85–91.PubMedCrossRefGoogle Scholar
  56. Shapiro, S. L. (2001). Quality of life and breast cancer: Relationship to psychosocial variables. J. Clin. Psychol. 57: 501–519.PubMedCrossRefGoogle Scholar
  57. Sikes, C. R. A., and Lasley, B. J. (1989). Cognitive sequelae of hypothalamic-pituitary-adrenal (HPA) dysregulation in depression. Biol. Psychiatr. 25: 148A–149A.CrossRefGoogle Scholar
  58. Speca, M., Carlson, L. E., Goodey, E., and Angen, M. (2000). A randomized, wait-list controlled clinical trial: the effect of a mindfulness meditation-based stress reduction program on mood and symptoms of stress in cancer outpatients. Psychosom. Med. 62: 613–622.PubMedGoogle Scholar
  59. Speilberger, C. D. (1983). Manual for the State-Trait Anxiety Inventory: STAI (Form Y). Consulting Psychologists Press, Palo Alto, CA.Google Scholar
  60. Spiegel, D., and Sephton, S. E. (2001). Psychoneuroimmune and endocrine pathways in cancer: effects of stress and support. Semin. Clini. Neuropsychiatr. 6: 252–265.CrossRefGoogle Scholar
  61. Spiegel, D., Sephton, S. E., Terr, A. I., and Sittes, D. P. (1998). Effects of psychosocial treatment in prolonging cancer survival may be mediated by neuroimmune pathways. Ann. New York Acad. Sci. 840: 674–683.CrossRefGoogle Scholar
  62. Tamarkin, L., Danforth, D., Lichter, A., DeMoss, E., Cohen, M., Chabner, B., et al. (1982). Decreased nocturnal plasma melatonin peak in patients with estrogen receptor positive breast cancer. Science 216: 1003–1005.PubMedCrossRefGoogle Scholar
  63. Ticher, A., Haus, E., Ron, I. G., Sackett-Lundeen, L., and Ashkenazi, I. E. (1996). The pattern of hormonal circadian time structure (acrophase) as an assessor of breast-cancer risk. Int. J. Cancer 65: 591–593.PubMedCrossRefGoogle Scholar
  64. Touitou, Y., Bogdan, A., Levi, F., Benavides, M., and Auzeby, A. (1996). Disruption of the circadian patterns of serum cortisol in breast and ovarian cancer patients: relationships with tumour marker antigens. Br. J. Cancer 74: 1248–1252.PubMedGoogle Scholar
  65. Turner-Cobb, J. M., Sephton, S. E., Koopman, C., Blake-Mortimer, J., and Spiegel, D. (2000). Social support and salivary cortisol in women with metastatic breast cancer. Psychosom. Med. 62: 337–345.PubMedGoogle Scholar
  66. van Der Pompe, G., Antoni, M. H., and Heijnen, C. J. (1996). Elevated basal cortisol levels and attenuated ACTH and cortisol responses to a behavioral challenge in women with metastatic breast cancer. Psychoneuroendocrinology 21: 361–374.PubMedCrossRefGoogle Scholar
  67. Vedhara, K., Miles, J., Bennett, P., Plummer, S., Tallon, D., Brooks, E., et al. (2003). An investigation into the relationship between salivary cortisol, stress, anxiety and depression. Biol. Psychol. 62: 89–96.PubMedCrossRefGoogle Scholar
  68. Vedhara, K., Stra, J. T., Miles, J. N., Sanderman, R., and Ranchor, A. V. (2006). Psychosocial factors associated with indices of cortisol production in women with breast cancer and controls. Psychoneuroendocrinology, 31: 299–311.PubMedCrossRefGoogle Scholar
  69. Vijayalaxmi, Meltz, M. L., Reiter, R. J., and Herman, T. S. (1999). Melatonin and protection from genetic damage in blood and bone marrow: whole-body irradiation studies in mice. J. Pineal Res. 27: 221–225.Google Scholar
  70. Vijayalaxmi, Reiter, R. J., Meltz, M. L., and Herman, T. S. (1998). Melatonin: possible mechanisms involved in its ‘radioprotective’ effect. Mutation Res. 404: 187–189.Google Scholar
  71. Vijayalaxmi, Thomas, C. R., Jr., Reiter, R. J., and Herman, T. S. (2002). Melatonin: from basic research to cancer treatment clinics. J Clin. Oncology 20: 2575–2601.Google Scholar
  72. White, I. R., Brunner, E. J., and Barron, J. L. (1995). A comparison of overnight and 24 hour collection to measure urinary catecholamines. J. Clin. Epidemiology 48: 263–267.CrossRefGoogle Scholar
  73. Wolkowitz, O. M. (1994). Prospective controlled studies of the behavioral and biological effects of exogenous corticosteroids. Psychoneuroendocrinology 3: 233–255.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Linda E. Carlson
    • 1
    • 2
    • 4
  • Tavis S. Campbell
    • 2
  • Sheila N. Garland
    • 2
  • Paul Grossman
    • 3
  1. 1.Department of OncologyFaculty of Medicine, University of CalgaryCalgaryCanada
  2. 2.Department of PsychologyUniversity of CalgaryCalgaryCanada
  3. 3.Freibugh Institute for Mindfulness Research, University of FreibughFreibughGermany
  4. 4.Department of Psychosocial ResourcesTom Baker Cancer CentreCalgaryCanada

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