Cortisol and inflammatory processes in ovarian cancer patients following primary treatment: Relationships with depression, fatigue, and disability

Brain, Behavior, and Immunity

Volumn 30, Issue SUPPL., 2013, Pages

  Schrepf, Andrew ^a   Clevenger, Lauren ^a   Christensen, Desire ^a   DeGeest, Koen ^b   Bender, David ^b   Ahmed, Amina ^b   Goodheart, Michael J ^b,c   Dahmoush, Laila ^b   Penedo, Frank ^d   Lucci, Joseph A ^d   Ganjei Azar, Parvin ^d   Mendez, Luis ^e   Markon, Kristian ^a   Lubaroff, David M ^a,b,c   Thaker, Premal H ^f   Slavich, George M ^g   Sood, Anil K ^h   Lutgendorf, Susan K ^a,b,c  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^d UNIVERSITY OF MIAMI   (United States)

^e FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Cortisol; Depression; Disability; Fatigue; IL 6; Inflammation; Ovarian cancer

Indexed keywords

HYDROCORTISONE; INTERLEUKIN 6;

ADULT; ARTICLE; CANCER CHEMOTHERAPY; CIRCADIAN RHYTHM; CYTOKINE RESPONSE; DEPRESSION; DISABILITY; DISEASE ASSOCIATION; FATIGUE; FEMALE; HORMONE RELEASE; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; OUTCOME ASSESSMENT; OVARY CANCER; PRIORITY JOURNAL; SELF REPORT; SLEEP;

AGED; CIRCADIAN RHYTHM; DEPRESSION; DISABLED PERSONS; FATIGUE; FEMALE; HUMANS; HYDROCORTISONE; INFLAMMATION; INTERLEUKIN-6; MIDDLE AGED; OVARIAN NEOPLASMS; QUALITY OF LIFE; SALIVA; SELF REPORT; STRESS, PSYCHOLOGICAL;

EID: 84875367955     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.07.022     Document Type: Article

References (87)

1. Abercrombie H.C., Giese-Davis J., Sephton S., Epel E.S., Turner-Cobb J.M., Spiegel D. Flattened cortisol rhythms in metastatic breast cancer patients. Psychoneuroendocrinology 2004, 29:1082-1092.
2. Alesci S., Martinez P.E., Kelkar S., Ilias I., Ronsaville D.S., Listwak S.J., Ayala A.R., Licinio J., Gold H.K., Kling M.A., Chrousos G.P., Gold P.W. Major depression is associated with significant diurnal elevations in plasma interleukin-6 levels, a shift of its circadian rhythm, and loss of physiological complexity in its secretion: clinical implications. J. Clin. Endocrinol. Metab. 2005, 90:2522-2530.
3. Bower J.E., Ganz P.A., Dickerson S.S., Petersen L., Aziz N., Fahey J.L. Diurnal cortisol rhythm and fatigue in breast cancer survivors. Psychoneuroendocrinology 2005, 30:92-100.
4. Bristow R.E., Tomacruz R.S., Armstrong D.K., Trimble E.L., Montz F.J. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J. Clin. Oncol. 2002, 20:1248-1259.
5. Campbell J., Ehlert U. Acute psychosocial stress: does the emotional stress response correspond with physiological responses?. Psychoneuroendocrinology 2012, (Epub ahead of print).
6. Chrousos G.P., Gold P.W. A healthy body in a healthy mind-and vice versa-the damaging power of " Uncontrollable" stress. J. Clin. Endocrinol. Metab. 1998, 83:1842-1845.
7. Clendenen T.V., Lundin E., Zeleniuch-Jacquotte A., Koenig K.L., Berrino F., Lukanova A., Lokshin A.E., Idahl A., Ohlson N., Hallmans G., Krogh V., Sieri S., Muti P., Marrangoni A., Nolen B.M., Liu M., Shore R.E., Arslan A.A. Circulating inflammation markers and risk of epithelial ovarian cancer. Cancer Epidemiol Biomarkers Prev. 2011, 20:799-810.
8. Colotta F., Allavena P., Sica A., Garlanda C., Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009, 30:1073-1081.
9. Conti B., Tabarean I., Andrei C., Bartfai T. Cytokines and fever. Front. Biosci. 2004, 9:1433-1449.
10. Curran S.L., Andrykowski M.A., Studts J.L. Short Form of the Profile of Mood States (POMS-SF): Psychometric information. Psychol. Assess. 1995, 7:80-83.
11. Dallman M.F., Akana S.F., Bhatnagar S., Bell M.E., Strack A.M. Bottomed out: metabolic significance of the circadian trough in glucocorticoid concentrations. Int. J. Obes. Relat. Metab. Disord. 2000, 24(Suppl 2):S40-6.
12. Dantzer R. Cytokine, sickness behavior, and depression. Neurol. Clin. 2006, 24:441-460.
13. Dantzer R., Wollman E.E., Yirmiya R. Cytokines and depression: an update. Brain Behav. Immun. 2002, 16:501-502.
14. De Jongh R.F., Vissers K.C., Meert T.F., Booij L.H.D.J., De Deyne C.S., Heylen R.J. The Role of interleukin-6 in nociception and pain. Anesth. Analg. 2003, 96:1096-1103.
15. de Oliveira C.M.B., Sakata R.K., Issy A.M., Gerola L.R., Salomão R. Cytokines and pain. Braz. J. Anesthesiol. 2011, 61:255-265.
16. Deuschle M., Gotthardt U., Schweiger U., Weber B., Körner A., Schmider J., Standhardt H., Lammers C.H., Heuser I. With aging in humans the activity of the hypothalamus-pituitary-adrenal system increases and its diurnal amplitude flattens. Life Sci. 1997, 61:2239-2246.
17. Dowlati Y., Herrmann N., Swardfager W., Liu H., Sham L., Reim E.K., Lanctôt K.L. A meta-analysis of cytokines in major depression. Biol. Psychiatry 2010, 67:446-457.
18. Edgell T., Martin-Roussety G., Barker G., Autelitano D.J., Allen D., Grant P., Rice G.E. Phase II biomarker trial of a multimarker diagnostic for ovarian cancer. J. Cancer Res. Clin. Oncol. 2010, 136:1079-1088.
19. Ershler W.B., Sun W.H., Binkley N., Gravenstein S., Volk M.J., Kamoske G., Klopp R.G., Roecker E.B., Daynes R.A., Weindruch R. Interleukin-6 and aging: blood levels and mononuclear cell production increase with advancing age and in vitro production is modifiable by dietary restriction. Lymphokine Cytok. Res. 1993, 12:225-230.
20. Fain J.N. Release of inflammatory mediators by human adipose tissue is enhanced in obesity and primarily by the nonfat cells: a review. Mediat. Inflamm. 2010, (Epub 2010).
21. Ferrucci L., Harris T.B., Guralnik J.M., Tracy R.P., Corti M.C., Cohen H.J., Penninx B., Pahor M., Wallace R., Havlik R.J. Serum IL-6 level and the development of disability in older persons. J. Am. Geriatr. Soc. 1999, 47:639-646.
22. Filipski E., Lévi F. Circadian disruption in experimental cancer processes. Integr. Cancer Ther. 2009, 8:298-302.
23. Fox S.W., Lyon D. Symptom clusters and quality of life in survivors of ovarian cancer. Cancer Nurs. 2007, 30:354-361.
24. Giacalone A., Polesel J., De Paoli A., Colussi A.M., Sartor I., Talamini R., Tirelli U. Assessing cancer-related fatigue: the psychometric properties of the revised piper fatigue scale in Italian cancer inpatients. Support Care Cancer 2010, 18:1191-1197.
25. Howren M.B., Lamkin D.M., Suls J. Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosom. Med. 2009, 71:171-186.
26. Illan-Gomez F., Gonzalvez-Ortega M., Orea-Soler I., Alcaraz-Tafalla M.S., Aragon-Alonso A., Pascual-Diaz M., Pérez-Paredes M., Lozano-Almela M.L. Obesity and inflammation: change in adiponectin, C-reactive protein, tumour necrosis factor-alpha and interleukin-6 after bariatric surgery. Obes. Surg. 2012, 22:950-955.
27. Jeannin P., Duluc D., Delneste Y. IL-6 and leukemia-inhibitory factor are involved in the generation of tumor-associated macrophage: regulation by IFN-gamma. Immunotherapy 2011, 3:23-26.
28. Jehn C.F., Kuehnhardt D., Bartholomae A., Pfeiffer S., Krebs M., Regierer A.C., Schmid P., Possinger K., Flath B.C. Biomarkers of depression in cancer patients. Cancer 2006, 107:2723-2729.
29. Jehn C.F., Kuhnhardt D., Bartholomae A., Pfeiffer S., Schmid P., Possinger K., Flath B.C., Luftner D. Association of IL-6, hypothalamus-pituitary-adrenal axis function, and depression in patients with cancer. Integr. Cancer Ther. 2010, 9:270-275.
30. Kirschbaum C., Hellhammer D.H. Salivary cortisol in psychobiological research: an overview. Neuropsychobiology 1989, 22:150-169.
31. Kirschbaum C., Hellhammer D.H. Salivary Cortisol. Encyclopedia of Stress 2000, vol. 3. Academic press, Burlington, MA.
32. Kraemer H.C., Giese-Davis J., Yutsis M., O'Hara R., Neri E., Gallagher-Thompson D., Taylor C.B., Spiegel D. Design decisions to optimize reliability of daytime cortisol slopes in an older population. Am. J. Geriatr. Psychiatry 2006, 14:325-333.
33. Laird N.M., Ware J.H. Random-effects models for longitudinal data. Biometrics 1982, 38:963-974.
34. Lamkin D.M., Lutgendorf S.K., Lubaroff D., Sood A.K., Beltz T.G., Johnson A.K. Cancer induces inflammation and depressive-like behavior in the mouse: Modulation by social housing. Brain Behav. Immun. 2011, 25:555-564.
35. Lane D., Matte I., Rancourt C., Piche A. Prognostic significance of IL-6 and IL-8 ascites levels in ovarian cancer patients. BMC Cancer 2011, 11:210.
36. Littell R.C., Pendergast J., Natarajan R. Modelling covariance structure in the analysis of repeated measures data. Stat. Med. 2000, 19:1793-1819.
37. Liu Y., Ho R.C., Mak A. Interleukin (IL)-6, tumour necrosis factor alpha (TNF-α) and soluble interleukin-2 receptors (sIL-2R) are elevated in patients with major depressive disorder: a meta-analysis and meta-regression. J. Affect. Disord. 2011, (Epub ahead of print).
38. Locke D.E.C., Decker P.A., Sloan J.A., Brown P.D., Malec J.F., Clark M.M., Rummans T.A., Ballman K.V., Schaefer P.L., Buckner J.C. Validation of single-item linear analog scale assessment of quality of life in neuro-oncology patients. J. Pain Symptom Manag. 2007, 34:628-638.
39. Lopez-Duran N.L., Kovacs M., George C.J. Hypothalamic-pituitary-adrenal axis dysregulation in depressed children and adolescents: a meta-analysis. Psychoneuroendocrinology 2009, 34:1272-1283.
40. Lutgendorf S.K., Weinrib A.Z., Penedo F., Russell D., DeGeest K., Costanzo E.S., Henderson P.J., Sephton S.E., Rohleder N., Lucci J.A., Cole S., Sood A.K., Lubaroff D.M. Interleukin-6, cortisol, and depressive symptoms in ovarian cancer patients. J. Clin. Oncol. 2008, 26:4820-4827.
41. Macciò A., Madeddu C., Massa D., Astara G., Farci D., Melis G.B., Mantovani G. Interleukin-6 and leptin as markers of energy metabolicchanges in advanced ovarian cancer patients. J. Cell Mol. Med. 2009, 13:3951-3959.
42. Marques A.H., Silverman M.N., Sternberg E.M. Glucocorticoid dysregulations and their clinical correlates. Ann. NY Acad. Sci. 2009, 1179:1-18.
43. Mastorakos G., Chrousos G.P., Weber J.S. Recombinant interleukin-6 activates the hypothalamic-pituitary-adrenal axis in humans. J. Clin. Endocrinol. Metab. 1993, 77:1690-1694.
44. Melhem A., Yamada S.D., Fleming G.F., Delgado B., Brickley D.R., Wu W., Kocherginsky M., Conzen S.D. Administration of glucocorticoids to ovarian cancer patients is associated with expression of the anti-apoptotic genes SGK1 and MKP1/DUSP1 in ovarian tissues. Clin. Cancer Res. 2009, 15:3196-3204.
45. Mormont M.C., Lévi F. Circadian-system alterations during cancer processes: a review. Int. J. Cancer 1997, 70:241-247.
46. Morrow G.R., Hickok J.T., Andrews P.L.R., Stern R.M. Reduction in serum cortisol after platinum based chemotherapy for cancer: a role for the HPA axis in treatment-related nausea?. Psychophysiology 2002, 39:491.
47. Musselman D.L., Miller A.H., Porter M.R., Manatunga A., Gao F., Penna S., Pearce B.D., Landry J., Glover S., McDaniel J.S., Nemeroff C.B. Higher than normal plasma interleukin-6 concentrations in cancer patients with depression: preliminary findings. Am. J. Psychiatry 2001, 158:1252-1257.
48. Neeck G., Crofford L.J. Neuroendocrine perturbations in fibromyalgia and chronic fatigue syndrome. Rheum. Dis. Clin. North Am. 2000, 26:989-1002.
49. Ness R.B., Grisso J.A., Cottreau C., Klapper J., Vergona R., Wheeler J.E., Morgan M., Schlesselman J.J. Factors related to inflammation of the ovarian epithelium and risk of ovarian cancer. Epidemiology 2000, 11:111-117.
50. Nilsson M.B., Langley R.R., Fidler I.J. Interleukin-6, secreted by human ovarian carcinoma cells, is a potent proangiogenic cytokine. Cancer Res. 2005, 65:10794-10800.
51. Obata N.H., Tamakoshi K., Shibata K., Kikkawa F., Tomoda Y. Effects of interleukin-6 on in vitro cell attachment, migration and invasion of human ovarian carcinoma. Anticancer Res. 1997, 17:337-342.
52. Offner F.A., Obrist P., Stadlmann S., Feichtinger H., Klinger P., Herold M., Zwierzina H., Hittmair A., Mikuz G., Abendstein B., Zeimet A., Marth C. Il-6 secretion by human peritoneal mesothelial and ovarian cancer cells. Cytokine 1995, 7:542-547.
53. Palesh O., Zeitzer J.M., Conrad A., Giese-Davis J., Mustian K.M., Popek V., Nga K., Spiegel D. Vagal regulation, cortisol, and sleep disruption in women with metastatic breast cancer. J. Clin. Sleep Med. 2008, 4:441-449.
54. Pan D., Kocherginsky M., Conzen S.D. Activation of the glucocorticoid receptor is associated with poor prognosis in estrogen receptor-negative breast cancer. Cancer Res. 2011, 71:6360-6370.
55. Pang D., Kocherginsky M., Krausz T., Kim S.Y., Conzen S.D. Dexamethasone decreases xenograft response to paclitaxel through inhibition of tumor cell apoptosis. Cancer Biol. Ther. 2006, 58:933-940.
56. Perlstein R.S., Mougey E.H., Jackson W.E., Neta R. Interleukin-1 and interleukin-6 act synergistically to stimulate the release of adrenocorticotropic hormone in vivo. Lymphokine Cytokine Res. 1991, 101-2:141-146.
57. Plante M., Rubin S.C., Wong G.Y., Federici M.G., Finstad C.L., Gastl G.A. Interleukin-6 level in serum and ascites as a prognostic factor in patients with epithelial ovarian cancer. Cancer 1994, 73:1882-1888.
58. Pyter L.M., Pineros V., Galang J.A., McClintock M.K., Prendergast B.J. Peripheral tumors induce depressive-like behaviors and cytokine production and alter hypothalamic-pituitary-adrenal axis regulation. Proc. Natl. Acad. Sci. USA 2009, 106:9069-9074.
59. Radloff L.S. The CES-D Scale: A self-report depression scale for research in the general population. Appl. Psychol. Meas. 1977, 1:385-401.
60. Rae M.T., Hillier S.G. Steroid signalling in the ovarian surface epithelium. Trends Endocrinol. Metab. 2005, 16:327-333.
61. Redwine L., Hauger R.L., Gillin J.C., Irwin M. Effects of sleep and sleep deprivation on interleukin-6, growth hormone, cortisol, and melatonin levels in humans. J. Clin. Endocrinol. Metab. 2000, 85:3597-3603.
62. Rhen T., Cidlowski J.A. Antiinflammatory action of glucocorticoids-new mechanisms for old drugs. N. Engl. J. Med. 2005, 353:1711-1723.
63. Scambia G., Testa U., Panici P.B., Foti E., Martucci R., Gadducci A., Perillo A., Facchini V., Peschle C., Mancuso S. Prognostic significance of interleukin 6 serum levels in patients with ovarian cancer. Br. J. Cancer 1995, 71:354-356.
64. Schlossmacher G., Stevens A., White A. Glucocorticoid receptor-mediated apoptosis: mechanisms of resistance in cancer cells. J. Endocrinol. 2011, 211:17-25.
65. Sephton S.E., Dhabhar F.S., Keuroghlian A.S., Giese-Davis J., McEwen B.S., Ionan A.C., Spiegel D. Depression, cortisol, and suppressed cell-mediated immunity in metastatic breast cancer. Brain Behav. Immun. 2009, 23:1148-1155.
66. Sephton S.E., Sapolsky R.M., Kraemer H.C., Spiegel D. Diurnal cortisol rhythm as a predictor of breast cancer survival. JNCI 2000, 92:994-1000.
67. Sergi G., Sarti S., Mosele M., Ruggiero E., Imoscopi A., Miotto F., Bolzetta F., Inelmen E.M., Manzato E., Coin A. Changes in healthy elderly women's physical performance. A 3-year follow-up. Exp. Gerontol. 2011, 46:929-933.
68. Sheehan T.J., Fifield J., Reisine S., Tennen H. The measurement structure of the Center for Epidemiologic Studies Depression Scale. J. Pers. Assess. 1995, 64:507-521.
69. Siervo M., Ruggiero D., Sorice R., Nutile T., Aversano M., Iafusco M., Vetrano F., Wells J.C., Stephan B.C., Ciullo M. Body mass index is directly associated with biomarkers of angiogenesis and inflammation in children and adolescents. Nutrition 2012, 28:262-266.
70. Sparkman N.L., Buchanan J.B., Heyen J.R., Chen J., Beverly J.L., Johnson R.W. Interleukin-6 facilitates lipopolysaccharide-induced disruption in working memory and expression of other proinflammatory cytokines in hippocampal neuronal cell layers. J. Neurosci. 2006, 26:10709-10716.
71. Stetler C., Miller G.E. Depression and hypothalamic-pituitary-adrenal activation: a quantitative summary of four decades of research. Psychosom. Med. 2011, 73:114-126.
72. Tempfer C., Zeisler H., Sliutz G., Haeusler G., Hanzal E., Kainz C. Serum evaluation of interleukin 6 in ovarian cancer patients. Gynecol. Oncol. 1997, 66:27-30.
73. Terreni L., De Simoni M.G. Role of the brain in interleukin-6 modulation. Neuroimmunomodulation 1998, 5:214-219.
74. Thornton L.M., Carson W.E., Shapiro C.L., Farrar W.B., Andersen B.L. Delayed emotional recovery after taxane-based chemotherapy. Cancer 2008, 113:638-647.
75. Touitou Y., Bogdan A., Levi F., Benavides M., Auzeby A. Disruption of the circadian patterns of serum cortisol in breast and ovarian cancer patients: relationships with tumour marker antigens. Br. J. Cancer 1996, 748:1248-1252.
76. Tsigos C., Chrousos G.P. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J. Psychosom. Res. 2002, 534:865-871.
77. Vegiopoulos A., Herzig S. Glucocorticoids, metabolism and metabolic diseases. Mol. Cell Endocrinol. 2007, 275:43-61.
78. Vgontzas A.N., Mastorakos G., Bixler E.O., Kales A., Gold P.W., Chrousos G.P. Sleep deprivation effects on the activity of the hypothalamic pituitary adrenal and growth axes: potential clinical implications. Clin. Endocrinol. (Oxford, UK) 1999, 51:205-215.
79. Vgontzas A.N., Bixler E.O., Lin H.M., Prolo P., Trakada G., Chrousos G.P. IL-6 and its circadian secretion in humans. Neuroimmunomodulation 2005, 12:131-140.
80. von Gruenigen V.E., Frasure H.E., Jenison E.L., Hopkins M.P., Gil K.M. Longitudinal assessment of quality of life and lifestyle in newly diagnosed ovarian cancer patients: the roles of surgery and chemotherapy. Gynecol. Oncol. 2006, 103:120-126.
81. Watson J.M., Sensintaffar J.L., Berek J.S., Martinez-Maza O. Constitutive production of interleukin 6 by ovarian cancer cell lines and by primary ovarian tumor cultures. Cancer Res. 1990, 50:6959-6965.
82. Weinrib A.Z., Sephton S.E., DeGeest K., Penedo F., Bender D., Zimmerman B., Kirschbaum C., Sood A.K., Lubaroff D.M., Lutgendorf S.K. Diurnal cortisol dysregulation, functional disability, and depression in women with ovarian cancer. Cancer 2010, 116:4410-4419.
83. Weitzman E.D., Zimmerman J.C., Czeisler C.A., Ronda J. Cortisol secretion is inhibited during sleep in normal man. J. Clin. Endocrinol. Metab. 1983, 56:352-358.
84. Wenzel L.B., Huang H.Q., Armstrong D.K., Walker J.L., Cella D. Health-related quality of life during and after intraperitoneal versus intravenous chemotherapy for optimally debulked ovarian cancer: a gynecologic oncology group study. J. Clin. Oncol. 2007, 25:437-443.
85. Wu S., Rodabaugh K., Martinez-Maza O., Watson J.M., Silberstein D.S., Boyer C.M., Peters W.P., Weinberg J.B., Berek J.S., Bast R.C. Stimulation of ovarian tumor cell proliferation with monocyte products inducing interleukin 1, interleukin 6 and tumor necrosis factor-alpha. Am. J. Obstet. Gynecol. 1992, 166:977-1007.
86. Zakrzewska I., Poznanski J. Changes of serum il-6 and CRP after chemotherapy in patients with ovarian carcinoma. [Zmiany stezenia IL-6 i CRP w surowicy chorych na nablonkowe nowotwory jajnika po leczeniu cytostatycznym]. Pol Merkur. Lekarski. 2001, 11:210-213.
87. Zhou D., Shanks N., Riechman S.E., Liang R., Kusnecov A.W., Rabin B.S. Interleukin 6 modulates interleukin-1-and stress-induced activation of the hypothalamic-pituitary-adrenal axis in male rats. Neuroendocrinology 1996, 63:227-236.