Psychologic stress, reduced NK cell activity, and cytokine dysregulation in women experiencing diagnostic breast biopsy

Psychoneuroendocrinology

Volumn 32, Issue 1, 2007, Pages 22-35

  Witek Janusek, Linda ^a   Gabram, Sheryl ^b   Mathews, Herbert L ^c  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b LOYOLA UNIVERSITY HEALTH SYSTEM   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Anxiety; Breast biopsy; Cytokines; Mood disturbance; NK cell activity; Perceived stress

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6;

ADAPTATION; ADULT; ANXIETY; ARTICLE; BENIGN TUMOR; BREAST BIOPSY; BREAST CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREGULATION; INTERFERON PRODUCTION; MAJOR CLINICAL STUDY; MALIGNANT NEOPLASTIC DISEASE; MENTAL STRESS; MOOD DISORDER; NATURAL KILLER CELL; PRIORITY JOURNAL; PSYCHOLOGICAL ASPECT;

AFFECT; AGED; ANXIETY; BIOPSY; BREAST NEOPLASMS; CYTOKINES; FEMALE; HUMANS; KILLER CELLS, NATURAL; MIDDLE AGED; NEUROIMMUNOMODULATION; STRESS, PSYCHOLOGICAL;

EID: 33845647278     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2006.09.011     Document Type: Article

References (92)

1. Agarwal S.K., and Marshall Jr. G.D. Dexamethasone promotes type 2 cytokine production primarily through inhibition of type 1 cytokines. J. Interferon Cytokine Res. 21 (2001) 147-155
2. Albertsson P.A., Basse P.H., Hokland M., Goldfarb R.H., Nagelkerke J.F., Nannmark U., and Kuppen P.J. NK cells and the tumour microenvironment: implications for NK-cell function and anti-tumour activity. Trends Immunol. 24 (2003) 603-609
3. Allavena P., Bianchi G., Paganin C., Giardina G., and Mantovani A. Regulation of adhesion and transendothelial migration of natural killer cells. Nat. Immun. 15 (1996) 107-116
4. Andersen B.L., Farrar W.B., Golden-Kreutz D., Kutz L.A., Maccallum R., Courtney M.E., and Glaser R. Stress and immune responses after surgical treatment for regional breast cancer. J. Natl. Cancer Inst. 90 (1998) 30-36
5. Andersen B.L., Kiecolt-Glaser J.K., and Glaser R. A biobehavioral model of cancer stress and disease course. Am. Psychol. 49 (1994) 389-404
6. Anderson B.L. Surviving cancer. Cancer 74 (1994) 1484-1495
7. Andrykowski M.A., Carpenter J.S., Studts J.L., Cordova M.J., Cunningham L.L., Beacham A., Sloan D., Kenady D., and Mcgrath P. Psychological impact of benign breast biopsy: a longitudinal, comparative study. Health Psychol. 21 (2002) 485-494
8. Barg F.K., Cooley M., Pasacreta J., Senay B., and McCorkle R. Development of a self-administered psychosocial cancer screening tool. Cancer Practice 2 (1994) 288-296
9. Barton M.B., Morley D.S., Moore S., Allen J.D., Kleinman K.P., Emmons K.M., and Fletcher S.W. Decreasing women's anxieties after abnormal mammograms: a controlled trial. J. Natl. Cancer Inst. 96 (2004) 529-538
10. Benedict S., Williams R.D., and Baron P.L. Recalled anxiety: from discovery to diagnosis of a benign breast mass. Oncol. Nurs. Forum. 21 (1994) 1723-1727
11. Benschop R.J., Rodriguez-Feuerhahn M., and Schedlowski M. Catecholamine-induced leukocytosis: early observations, current research, and future directions. Brain Behav. Immun. 10 (1996) 77-91
12. Biondi M. Effects of stress on immune functions: an overview. In: Ader R., and Cohen N. (Eds). Psychoneuroimmunology vol. 2 (2001), Academic Press, New York 189-226
13. Biron C.A. Initial and innate responses to viral infections-pattern setting in immunity or disease. Curr. Opin. Microbiol. 2 (1999) 374-381
14. Biron C.A., Nguyen K.B., Pien G.C., Cousens L.P., and Salazar-Mather T.P. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17 (1999) 189-220
15. Bosch J.A., Berntson G.G., Cacioppo J.T., and Marucha P.T. Differential mobilization of functionally distinct natural killer subsets during acute psychologic stress. Psychosom. Med. 67 (2005) 366-375
16. Brett, J., 1999. A multi-centre follow-up study to assess the anxiety and opinions of women 1 month before their next routine breast screening appointment having previously attended three years later. J. Sc. Dissertation.
17. Brett J., and Austoker J. Women who are recalled for further investigation for breast screening: psychological consequences 3 years after recall and factors affecting re-attendance. J. Public Health Med. 23 (2001) 292-300
18. Brett J., Austoker J., and Ong G. Do women who undergo further investigation for breast screening suffer adverse psychological consequences? A multi-centre follow-up study comparing different breast screening result groups five months after their last breast screening appointment. J. Public Health Med. 20 (1998) 396-403
19. Brosschot J.F., Benschop R.J., Godaert G.L., De Smet M.B., Olff M., Heijnen C.J., and Ballieux R.E. Effects of experimental psychological stress on distribution and function of peripheral blood cells. Psychosom. Med. 54 (1992) 394-406
20. Cannon G.B., Dean J.H., Herberman R.B., Perlin E., Reid J., Miller C., and Lang N.P. Association of depressed postoperative lymphoproliferative responses to alloantigens with poor prognosis in patients with stage I lung cancer. Int. J. Cancer 25 (1980) 9-17
21. Charmandari E., Tsigos C., and Chrousos G. Endocrinology of the stress response. Annu. Rev. Physiol. 67 (2005) 259-284
22. Chrousos G.P. The stress response and immune function: clinical implications. The 1999 Novera H. Spector Lecture. Ann. NY Acad. Sci. 917 (2000) 38-67
23. Cohen S., Kamarck T., and Mermelstein R. A global measure of perceived stress. J. Health Soc. Behav. 24 (1983) 31-67
24. Cooper M.A., Fehniger T.A., and Caligiuri M.A. The biology of human natural killer-cell subsets. Trends Immunol. 22 (2001) 633-640
25. Cooper M.A., Fehniger T.A., Turner S.C., Chen K.S., Ghaheri B.A., Ghayur T., Carson W.E., and Caligiuri M.A. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood 97 (2001) 3146-3151
26. Daynes R.A., Araneo B.A., Dowell T.A., Huang K., and Dudley D. Regulation of murine lymphokine production in vivo. III. The lymphoid tissue microenvironment exerts regulatory influences over T helper cell function. J. Exp. Med. 171 (1990) 979-996
27. Deane K.A., and Degner L.F. Information needs, uncertainty, and anxiety in women who had a breast biopsy with benign outcome. Cancer Nurs. 21 (1998) 117-126
28. Diefenbach A., and Raulet D.H. The innate immune response to tumors and its role in the induction of T-cell immunity. Immunol. Rev. 188 (2002) 9-21
29. Drageset S., and Lindstrom T.C. The mental health of women with suspected breast cancer: the relationship between social support, anxiety, coping and defence in maintaining mental health. J. Psychiatr. Ment. Health Nurs. 10 (2003) 401-409
30. Elenkov I.J. Glucocorticoids and the Th1/Th2 balance. Ann. NY Acad. Sci. 1024 (2004) 138-146
31. Elenkov I.J., and Chrousos G.P. Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann. NY Acad. Sci. 966 (2002) 290-303
32. Esterling B.A., Kiecolt-Glaser J.K., Bodnar J.C., and Glaser R. Chronic stress, social support, and persistent alterations in the natural killer cell response to cytokines in older adults. Health Psychol. 13 (1994) 291-298
33. Esterling B.A., Kiecolt-Glaser J.K., and Glaser R. Psychosocial modulation of cytokine-induced natural killer cell activity in older adults. Psychosom. Med. 58 (1996) 264-272
34. Fawzy F.I., Kemeny M.E., Fawzy N.W., Elashoff R., Morton D., Cousins N., and Fahey J.L. A structured psychiatric intervention for cancer patients. II. Changes over time in immunological measures. Arch. Gen. Psychiatry 47 (1990) 729-735
35. Gabriel H., Schwarz L., Steffens G., and Kindermann W. Immunoregulatory hormones, circulating leucocyte and lymphocyte subpopulations before and after endurance exercise of different intensities. Int. J .Sports Med. 13 (1992) 359-366
36. Ghosh K., Melton III L.J., Suman V.J., Grant C.S., Sterioff S., Brandt K.R., Branch C., Sellers T.A., and Hartmann L.C. Breast biopsy utilization: a population-based study. Arch. Intern. Med. 165 (2005) 1593-1598
37. Glaser R. Stress-associated immune dysregulation and its importance for human health: a personal history of psychoneuroimmunology. Brain Behav. Immun. 19 (2005) 3-11
38. Hughson A.V., Cooper A.F., Mcardle C.S., and Smith D.C. Psychosocial morbidity in patients awaiting breast biopsy. J. Psychosom. Res. 32 (1988) 173-180
39. Irwin M., Daniels M., Bloom E.T., Smith T.L., and Weiner H. Life events, depressive symptoms, and immune function. Am. J. Psychiatry 144 (1987) 437-441
40. Kiecolt-Glaser J.K., Glaser R., Strain E.C., Stout J.C., Tarr K.L., Holliday J.E., and Speicher C.E. Modulation of cellular immunity in medical students. J. Behav. Med. 9 (1986) 5-21
41. Kiecolt-Glaser J.K., Glaser R., Shuttleworth E.C., Dyer C.S., Ogrocki P., and Speicher C.E. Chronic stress and immunity in family caregivers of Alzheimer's disease victims. Psychosom. Med. 49 (1987) 523-535
42. Kiecolt-Glaser J.K., Dura J.R., Speicher C.E., Trask O.J., and Glaser R. Spousal caregivers of dementia victims: longitudinal changes in immunity and health. Psychosom. Med. 53 (1991) 345-362
43. Kiecolt-Glaser J.K., Malarkey W.B., Chee M., Newton T., Cacioppo J.T., Mao H.Y., and Glaser R. Negative behavior during marital conflict is associated with immunological down-regulation. Psychosom. Med. 55 (1993) 395-409
44. Lanier L.L. On guard-activating NK cell receptors. Nat. Immunol. 2 (2001) 23-27
45. Lanier L.L., Le A.M., Civin C.I., Loken M.R., and Phillips J.H. The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral blood NK cells and cytotoxic T lymphocytes. J. Immunol. 136 (1986) 4480-4486
46. Lebel S., Jakubovits G., Rosberger Z., Loiselle C., Seguin C., Cornaz C., Ingram J., August L., and Lisbona A. Waiting for a breast biopsy. Psychosocial consequences and coping strategies. J. Psychosom. Res. 55 (2003) 437-443
47. Levy S., Herberman R., Lippman M., and D'angelo T. Correlation of stress factors with sustained depression of natural killer cell activity and predicted prognosis in patients with breast cancer. J. Clin. Oncol. 5 (1987) 348-353
48. London L., Perussia B., and Trinchieri G. Induction of proliferation in vitro of resting human natural killer cells: IL 2 induces into cell cycle most peripheral blood NK cells, but only a minor subset of low density T cells. J. Immunol. 137 (1986) 3845-3854
49. Macfarlane M.E., and Sony S.D. Women, breast lump discovery, and associated stress. Health Care Women Int. 13 (1992) 23-32
50. Madden K.S., and Felten D.L. Experimental basis for neural-immune interactions. Physiol. Rev. 75 (1995) 77-106
51. Maes M., Lin A.H., Delmeire L., Van Gastel A., Kenis G., De Jongh R., and Bosmans E. Elevated serum interleukin-6 (IL-6) and IL-6 receptor concentrations in posttraumatic stress disorder following accidental man-made traumatic events. Biol. Psychiatry 45 (1999) 833-839
52. Maisel A.S., Harris T., Rearden C.A., and Michel M.C. Beta-adrenergic receptors in lymphocyte subsets after exercise. Alterations in normal individuals and patients with congestive heart failure. Circulation 82 (1990) 2003-2010
53. Manetti R., Parronchi P., Giudizi M.G., Piccinni M.P., Maggi E., Trinchieri G., and Romagnani S. Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med. 177 (1993) 1199-1204
54. Marshall Jr. G.D., Agarwal S.K., Lloyd C., Cohen L., Henninger E.M., and Morris G.J. Cytokine dysregulation associated with exam stress in healthy medical students. Brain Behav. Immun. 12 (1998) 297-307
55. Martin-Fontecha A., Thomsen L.L., Brett S., Gerard C., Lipp M., Lanzavecchia A., and Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat. Immunol. 5 (2004) 1260-1265
56. Matalka K.Z. Neuroendocrine and cytokines-induced responses to minutes, hours, and days of mental stress. Neuro Endocrinol. Lett. 24 (2003) 283-292
57. McEwen B.S., Biron C.A., Brunson K.W., Bulloch K., Chambers W.H., Dhabhar F.S., Goldfarb R.H., Kitson R.P., Miller A.H., Spencer R.L., and Weiss J.M. The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res. Brain Res. Rev. 23 (1997) 79-133
58. McNair D.M., Lorr M., and Droppleman L.F. Manual for the Profile of Mood States (1992), EdITS, San Diego
59. Montgomery G.H., David D., Goldfarb A.B., Silverstein J.H., Weltz C.R., Birk J.S., and Bovbjerg D.H. Sources of anticipatory distress among breast surgery patients. J. Behav. Med. 26 (2003) 153-164
60. Murray D.R., Irwin M., Rearden C.A., Ziegler M., Motulsky H., and Maisel A.S. Sympathetic and immune interactions during dynamic exercise. Mediation via a beta 2-adrenergic-dependent mechanism. Circulation 86 (1992) 203-213
61. Nagabhushan M., Mathews H.L., and Witek-Janusek L. Aberrant nuclear expression of ap-1 and nfkb in lymphocytes of women stressed by the experience of breast biopsy. Brain Behav. Immun. 15 (2001) 78-84
62. Nagler A., Lanier L.L., Cwirla S., and Phillips J.H. Comparative studies of human FcRIII-positive and negative natural killer cells. J. Immunol. 143 (1989) 3183-3191
63. Naliboff B.D., Benton D., Solomon G.F., Morley J.E., Fahey J.L., Bloom E.T., Makinodan T., and Gilmore S.L. Immunological changes in young and old adults during brief laboratory stress. Psychosom. Med. 53 (1991) 121-132
64. Northouse L.L., Jeffs M., Cracchiolo-Caraway A., Lampman L., and Dorris G. Emotional distress reported by women and husbands prior to a breast biopsy. Nurs. Res. 44 (1995) 196-201
65. O'mahony M. Women's lived experience of breast biopsy: a phenomenological study. J. Clin. Nurs. 10 (2001) 512-520
66. Ong G., Austoker J., and Brett J. Breast screening: adverse psychological consequences one month after placing women on early recall because of a diagnostic uncertainty. A multicentre study. J. Med. Screen 4 (1997) 158-168
67. Parronchi P., De Carli M., Manetti R., Simonelli C., Sampognaro S., Piccinni M.P., Macchia D., Maggi E., Del Prete G., and Romagnani S. IL-4 and IFN (alpha and gamma) exert opposite regulatory effects on the development of cytolytic potential by Th1 or Th2 human T cell clones. J. Immunol. 149 (1992) 2977-2983
68. Pross H.F., and Lotzova E. Role of natural killer cells in cancer. Nat. Immun. 12 (1993) 279-292
69. Reiter Z. Interferon-a major regulator of natural killer cell-mediated cytotoxicity. J. Interferon Res. 13 (1993) 247-257
70. Rennick D., Hunte B., Holland G., and Thompson-Snipes L. Cofactors are essential for stem cell factor-dependent growth and maturation of mast cell progenitors: comparative effects of interleukin-3 (IL-3), IL-4, IL-10, and fibroblasts. Blood 85 (1995) 57-65
71. Robertson M.J., and Ritz J. Biology and clinical relevance of human natural killer cells. Blood 76 (1990) 2421-2438
72. Rook G.A., Hernandez-Pando R., and Lightman S.L. Hormones, peripherally activated prohormones and regulation of the Th1/Th2 balance. Immunol. Today 15 (1994) 301-303
73. Sachs G., Rasoul-Rockenschaub S., Aschauer H., Spiess K., Gober I., Staffen A., and Zielinski C. Lytic effector cell activity and major depressive disorder in patients with breast cancer: a prospective study. J. Neuroimmunol. 59 (1995) 83-89
74. Sallusto F., Geginat J., and Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22 (2004) 745-763
75. Schedlowski M., Jacobs R., Alker J., Prohl F., Stratmann G., Richter S., Hadicke A., Wagner T.O., Schmidt R.E., and Tewes U. Psychophysiological, neuroendocrine and cellular immune reactions under psychological stress. Neuropsychobiology 28 (1993) 87-90
76. Segerstrom S.C., and Miller G.E. Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychol. Bull. 130 (2004) 601-630
77. Somersalo K. Migratory functions of natural killer cells. Nat. Immun. 15 (1996) 117-133
78. Spielberger, C.D., Gorsuch, R.C., Lushene, R.E., 1970. Manual for the State-Trait Anxiety Inventory, 457.
79. Stark D.P., and House A. Anxiety in cancer patients. Br. J. Cancer 83 (2000) 1261-1267
80. Street S.E., Cretney E., and Smyth M.J. Perforin and interferon-gamma activities independently control tumor initiation, growth, and metastasis. Blood 97 (2001) 192-197
81. Targan S., and Dorey F. Dual mechanism of interferon augmentation of natural killer cytotoxicity (NKCC). Ann. NY Acad. Sci. 350 (1980) 121-129
82. Trinchieri G. Biology of natural killer cells. Adv. Immunol. 47 (1989) 187-376
83. Tussey L., Speller S., Gallimore A., and Vessey R. Functionally distinct CD8+ memory T cell subsets in persistent EBV infection are differentiated by migratory receptor expression. Eur. J. Immunol. 30 (2000) 1823-1829
84. Van Den Broek M.E., Kagi D., Ossendorp F., Toes R., Vamvakas S., Lutz W.K., Melief C.J., Zinkernagel R.M., and Hengartner H. Decreased tumor surveillance in perforin-deficient mice. J. Exp. Med. 184 (1996) 1781-1790
85. Viswanathan K., and Dhabhar F.S. Stress-induced enhancement of leukocyte trafficking into sites of surgery or immune activation. Proc. Natl. Acad. Sci. USA 102 (2005) 5808-5813
86. Vose B.M., Riccardi C., Bonnard G.D., and Herberman R.B. Limiting dilution analysis of the frequency of human T cells and large granular lymphocytes proliferating in response to interleukin 2. II. Regulatory role of interferon on proliferative and cytotoxic precursors. J. Immunol. 130 (1983) 768-772
87. Weigent D., and Blalock J. Bidirectional communication between the immune and neuroendocrine systems. In: Plotnikoff N., Faith R., Murgot A., and Goods R. (Eds). Cytokines, Stress, and Immunity (1999), CRC Press, New York 173-186
88. Weisse C.S. Depression and immunocompetence: a review of the literature. Psychol. Bull. 111 (1992) 475-489
89. Whiteside T.L., and Herberman R.B. Role of human natural killer cells in health and disease. Clin. Diagn Lab. Immunol. 1 (1994) 125-133
90. Witek-Janusek L., and Mathews H. Stress, immunity, and health outcomes. In: Rice V. (Ed). Handbook of Stress, Coping, and Health. Implications for Nursing Research, Theory, and Practice (2000), Sage Publications, Thousand Oaks 47-67
91. Witek-Janusek L., and Mathews H.L. Differential effects of glucocorticoids on colony stimulating factors produced by neonatal mononuclear cells. Pediatr. Res. 45 (1999) 224-229
92. Zhang J., Scordi I., Smyth M.J., and Lichtenheld M.G. Interleukin 2 receptor signaling regulates the perforin gene through signal transducer and activator of transcription (Stat)5 activation of two enhancers. J. Exp. Med. 190 (1999) 1297-1308