Long lasting effects of smoking: Breast cancer survivors' inflammatory responses to acute stress differ by smoking history

Psychoneuroendocrinology

Volumn 38, Issue 2, 2013, Pages 179-187

  Bennett, Jeanette M ^a,b   Glaser, Ronald ^b   Andridge, Rebecca R ^a   Peng, Juan ^a   Malarkey, William B ^b   Kiecolt Glaser, Janice K ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Cancer survivors; Cortisol; Glucocorticoid resistance; Interleukin 6 (IL 6); Persistent inflammation; Smoking; Stress

Indexed keywords

ANTIDEPRESSANT AGENT; AROMATASE INHIBITOR; HYDROCORTISONE; INTERLEUKIN 6; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ACUTE STRESS; ADULT; ARTICLE; BREAST CANCER; CANCER STAGING; CANCER SURVIVOR; COMORBIDITY; CONTROLLED STUDY; DEPRESSION; FEMALE; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MENTAL STRESS; PRIORITY JOURNAL; SMOKING;

BREAST NEOPLASMS; FEMALE; HUMANS; HYDROCORTISONE; INFLAMMATION; INTERLEUKIN-6; MIDDLE AGED; PSYCHIATRIC STATUS RATING SCALES; SALIVA; SMOKING; STRESS, PSYCHOLOGICAL; SURVIVORS;

EID: 84872838097     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2012.05.012     Document Type: Article

References (71)

1. Aardal E., Holm A.C. Cortisol in saliva-reference ranges and relation to cortisol in serum. Clin. Chem. Lab. Med. 1995, 33:927-932.
2. Aggarwal B.B., Shishodia S., Sandur S.K., Pandey M.K., Sethi G. Inflammation and cancer: how hot is the link?. Biochem. Pharmacol. 2006, 72:1605-1621.
3. Agusti A., Noguera A., Sauleda J., Sala E., Pons J., Busquets X. Systemic effects of chronic obstructive pulmonary disease. Eur. Respir. J. 2003, 21:347-360.
4. al'Absi M., Wittmers L.E., Erickson J., Hatsukami D., Crouse B. Attenuated adrenocortical and blood pressure responses to psychological stress in ad libitum and abstinent smokers. Pharmacol. Biochem. Behav. 2003, 74:401-410.
5. Altemus M., Rao B., Dhabhar F.S., Ding W., Granstein R.D. Stress-induced changes in skin barrier function in healthy women. J. Invest. Dermatol. 2001, 117:309-317.
6. Backhaus J., Junghanns K., Broocks A., Riemann D., Hohagen F. Test-retest reliability and validity of the Pittsburgh Sleep Quality Index in primary insomnia. J. Psychosom. Res. 2002, 53:737-740.
7. Balfour D.J. Influence of nicotine on the release of monoamines in the brain. Prog. Brain Res. 1989, 79:165-172.
8. Barnes P.J. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin. Sci. 1998, 94:557-572.
9. Barnes P.J., Adcock I.M. Glucocorticoid resistance in inflammatory diseases. The Lancet 2009, 373:1905-1917.
10. Basco M.R., Krebaum S.R., Rush A.J. Outcome measures of depression. Measuring Patient Changes in Mood, Anxiety, and Personality Disorders 1997, 207-245. American Psychological Association, Washington, DC. H.H. Strupp, L.M. Horowitz, M.J. Lambert (Eds.).
11. Bazzano L., He J., Muntner P., Vupputuri S., Whelton P.K. Relationship between smoking and novel risk factors for cardiovascular disease in the United States. Ann. Intern. Med. 2003, 138:891-898.
12. Bermudez E.A., Rifai N., Buring J.E., Manson J.E., Ridker P.M. Relation between markers of systemic vascular inflammation and smoking in women. Am. J. Cardiol. 2002, 89:1117-1119.
13. Bo S., Gentile L., Ciccone G., Baldi C., Benini L., Dusio F., Lucia C., Forastiere G., Nuti C., Cassader M., Pagano G.F. The metabolic syndrome and high C-reactive protein: prevalence and differences by sex in a southern-European population-based cohort. Diabetes Metab. Res. 2005, 21:515-524.
14. Bower J.E. Cancer-related fatigue: links with inflammation in cancer patients and survivors. Brain Behav. Immun. 2007, 21:863-871.
15. Brattsand R., Linden M. Cytokine modulation by glucocorticoids: mechanisms and actions in cellular studies. Aliment. Pharm. Therap. 1996, 10:81-90.
16. Brydon L., Edwards S., Jia H.Y., Mohamed-Ali V., Zachary I., Martin J.F., Steptoe A. Psychological stress activates interleukin-1 beta gene expression in human mononuclear cells. Brain Behav. Immun. 2005, 19:540-546.
17. Buysse D.J., Reynolds C.F., Monk T.H., Berman S.R., Kupfer D.J. Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989, 28:193-213.
18. Center for Disease Control and Prevention (CDC) Tobacco use, access, and exposure to tobacco in media among middle and high school students - United States, 2004. MMWR 2005, 54:297-301.
19. Charlson M., Szatrowski T.P., Peterson J., Gold J. Validation of a combined comorbidity index. J. Clin. Epidemiol. 1994, 47:1245-1251.
20. Chaudhuri R., Livingston E., McMahon A.D., Thomson L., Borland W., Thomson N.C. Cigarette smoking impairs the therapeutic response to oral corticosteroids in chronic asthma. Am. J. Respir. Crit. Care Med. 2003, 168:1308-1311.
21. Childs E., de Wit H. Hormonal, cardiovascular, and subjective responses to acute stress in smokers. Psychopharmacology (Berl.) 2009, 203:1-12.
22. Cohen S., Kamarck T., Mermelstein R. A global measure of perceived stress. J. Health Soc. Behav. 1983, 24:385-396.
23. Cormet-Boyaka E., Jolivette K., Bonnegarde A., Rennolds J., Hassan F., Mehta P., Tridandapani S., Webster-Marketon J., Boyaka P.N. An NF-κB-independent and Erk1/2-dependent mechanism controls CXCL8/IL-8 responses of airway epithelial cells to cadmium. Toxicol Sci. 2012, 125:418-429.
24. Cross C.E., Traber M., Eiserich J., van der Vliet A. Micronutrient antioxidants and smoking. Br. Med. Bull. 1999, 55:691-704.
25. Das I. Raised C-reactive protein levels in serum from smokers. Clin. Chim. Acta 1985, 153:9-13.
26. Demark-Wahnefried W., Morey M.C., Clipp E.C., Pieper C.F., Snyder D.C., Sloane R., Cohen H.J. Leading the way in exercise and diet (Project LEAD): intervening to improve function among older breast and prostate cancer survivors. Control. Clin. Trials 2003, 24:206-223.
27. Diggle P.J., Heagerty P., Liang K.Y., Zeger S.L. Analysis of Longitudinal Data 2002, Clarendon Press, Oxford. 2nd ed.
28. Doll R., Peto R., Boreham J., Sutherland I. Mortality in relation to smoking: 50 years' observations on male British doctors. Br. Med. J. 2004, 328:1519.
29. Drum M.L., Shiovitz-Ezra S., Gaumer E., Lindau S.T. Assessment of smoking behaviors and alcohol use in the national social life, health, and aging project. J. Gerontol. B: Psychol. 2009, 64:I119-I130.
30. Edwards K.M., Burns V.E., Ring C., Carroll D. Sex differences in the interleukin-6 response to acute psychological stress. Biol. Psychol. 2006, 71:236-239.
31. Ershler W.B., Keller E.T. Age-associated increased interleukin-6 gene expression, late-life diseases, and frailty. Annu. Rev. Med. 2000, 51:245-270.
32. Frohlich M., Sund M., Lowel H., Imhof A., Hoffmeister A., Koenig W. Independent association of various smoking characteristics with markers of systemic inflammation in men - Results from a representative sample of the general population (MONICA Augsburg Survey 1994/95). Eur. Heart J. 2003, 24:1365-1372.
33. Glaser R., Robles T., Sheridan J., Malarkey W.B., Kiecolt-Glaser J.K. Mild depressive symptoms are associated with amplified and prolonged inflammatory responses following influenza vaccination in older adults. Arch. Gen. Psychiatry 2003, 60:1009-1014.
34. Haddy N., Sass C., Maumus S., Marie B., Droesch S., Siest G., Lambert D., Visvikis S. Biological variations, genetic polymorphisms and familial resemblance of TNF-alpha and IL-6 concentrations: STANISLAS cohort. Eur. J. Hum. Genet. 2005, 13:109-117.
35. Harris T., Ferrucci L., Tracy R., Corti M., Wacholder S., Ettinger W.J., Heimovitz H., Cohen H., Wallace R. Associations of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly. Am. J. Med. 1999, 106:506-512.
36. Härtl K., Janni W., Kästner R., Sommer H., Strobl B., Rack B., Stauber M. Impact of medical and demographic factors on long-term quality of life and body image of breast cancer patients. Ann. Oncol. 2003, 14:1064-1071.
37. Helmersson J., Larsson A., Vessby B., Basu S. Active smoking and a history of smoking are associated with enhanced prostaglandin F-2 alpha, interleukin-6 and F-2-isoprostane formation in elderly men. Atherosclerosis 2005, 181:201-207.
38. Jin T., Lu J., Nordberg M. Toxicokinetics and biochemistry of cadmium with special emphasis on the role of metallothionein. Neurotoxicology 1998, 19:529-535.
39. Kirschbaum C., Pirke K.M., Hellhammer D.H. The " Trier Social Stress Test" : a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 1993, 28:76-81.
40. Kirschbaum C., Scherer G., Strasburger C.J. Pituitary and adrenal hormone responses to pharmacological, physical, and psychological stimulation in habitual smokers and nonsmokers. Clin. Investig. 1994, 72:804-810.
41. Kirschbaum C., Strasburger C.J., Langkrar J. Attenuated cortisol response to psychological stress but not to CRH or ergometry in young habitual smokers. Pharmacol. Biochem. Behav. 1993, 44:527-531.
42. Krocova Z., Macela A., Kroca M., Hernychova L. The immunomodulatory effects of lead and cadmium on the cells of immune system in vitro. Toxicology In Vitro 2000, 14:33-40.
43. Kudielka B., Schommer N., Hellhammer D., Kirschbaum C. Acute HPA axis responses, heart rate, and mood changes to psychosocial stress (TSST) in humans at different times of day. Psychoneuroendocrinology 2004, 29:983-992.
44. Kunz-Ebrecht S.R., Mohamed-Ali V., Feldman P.J., Kirschbaum C., Steptoe A. Cortisol responses to mild psychological stress are inversely associated with proinflammatory cytokines. Brain Behav. Immun. 2003, 17:373-383.
45. Låg M., Rodionov D., Øvrevik J., Bakke O., Schwarze P.E., Refsnes M. Cadmium-induced inflammatory responses in cells relevant for lung toxicity: expression and release of cytokines in fibroblasts, epithelial cells and macrophages. Toxicol. Lett. 2010, 193:252-260.
46. McGregor B.A., Antoni M.H. Psychological intervention and health outcomes among women treated for breast cancer: a review of stress pathways and biological mediators. Brain Behav. Immun. 2009, 23:159-166.
47. Mendall M.A., Strachan D.P., Butland B.K., Ballam L., Morris J., Sweetnam P.M., Elwood P.C. C-reactive protein: relation to total mortality, cardiovascular mortality and cardiovascular risk factors in men. Eur. Heart J. 2000, 21:1584-1590.
48. Mendelson J.H., Sholar M.B., Goletiani N., Siegel A.J., Mello N.K. Effects of low-and high-nicotine cigarette smoking on mood states and the HPA axis in men. Neuropsychopharmacology 2005, 30:1751-1763.
49. Miller G., Cohen S., Ritchey A. Chronic psychological stress and the regulation of pro-inflammatory cytokines: a glucocorticoid-resistance model. Health Psychol. 2002, 21:531-541.
50. Nazmi A., Oliveira I.O., Victora C.G. Correlates of C-reactive protein levels in young adults: a population-based cohort study of 3827 subjects in Brazil. Braz. J. Med. Biol. Res. 2008, 41:357-367.
51. Owen N., Poulton T., Hay F.C., Mohamed-Ali V., Steptoe A. Socioeconomic status, C-reactive protein, immune factors, and responses to acute mental stress. Brain Behav. Immun. 2003, 17:286-295.
52. Pace T.W.W., Mletzko T.C., Alagbe O., Musselman D.L., Nemeroff C.B., Miller A.H., Heim C.M. Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress. Am. J. Psychiatry 2006, 163:1630-1632.
53. Pedersen B., Dahl R., Karlstrom R., Peterson C., Venge P. Eosinophil and neutrophil activity in asthma in a one-year trial with inhaled budesonide. The impact of smoking. Am. J. Respir. Crit. Care Med. 1996, 153:1519-1529.
54. Pierce B.L., Ballard-Barbash R., Bernstein L., Baumgartner R.N., Neuhouser M.L., Wener M.H., Baumgartner K.B., Gilliland F.D., Sorensen B.E., McTiernan A., Ulrich C.M. Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J. Clin. Oncol. 2009, 27:3437-3444.
55. Radloff L.S. The CES-D scale: a self-report depression scale for research in the general population. Appl. Psych. Meas. 1977, 1:385-401.
56. Rennolds J., Butler S., Maloney K., Boyaka P.N., Davis I.C., Knoell D.L., Parinandi N.L., Cormet-Boyaka E. Cadmium regulates the expression of the cftr chloride channel in human airway epithelial cells. Toxicol. Sci. 2010, 116:349-358.
57. Roberts R., Vernon S. The center for epidemiologic studies depression scale: its use in a community sample. Am. J. Psychiatry 1983, 140:41-46.
58. Rohleder N., Kirschbaum C. The hypothalamic-pituitary-adrenal (HPA) axis in habitual smokers. Int. J. Psychophysiol. 2006, 59:236-243.
59. Stein K.D., Jacobsen P.B., Blanchard C.M., Thors C. Further validation of the multidimensional fatigue symptom inventory-short form. J. Pain Symptom Manage. 2004, 27:14-23.
60. Stein K.D., Martin S.C., Hann D.M., Jacobsen P.B. A multidimensional measure of fatigue for use with cancer patients. Cancer Pract. 1998, 6:143-152.
61. Steptoe A., Hamer M., Chida Y. The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav. Immun. 2007, 21:901-912.
62. Steptoe A., Owen N., Kunz-Ebrecht S.R., Mohamed-Ali V. Inflammatory cytokines, socioeconomic status, and acute stress responsivity. Brain Behav. Immun. 2002, 16:774-784.
63. Steptoe A., Ussher M. Smoking, cortisol and nicotine. Int. J. Psychophysiol. 2006, 59:228-235.
64. Steptoe A., Willemsen G., Owen N., Flower L., Mohamed-Ali V. Acute mental stress elicits delayed increases in circulating inflammatory cytokine levels. Clin. Sci. 2001, 101:185-192.
65. United States Department of Health and Human Services (USDHHS) How Tobacco Smoke Causes Disease: The Biology and Behavioral Basis for Smoking-Attributable Disease: A Report of the Surgeon General 2010, U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health, Atlanta, GA.
66. Van den Beuken-van Everdingen M., Peters M.L., de Rijke J.M., Schouten H.C., van Kleef M., Patijn J. Concerns of former breast cancer patients about disease recurrence: a validation and prevalence study. Psychooncology 2008, 17:1137-1145.
67. von Kanel R., Kudielka B.M., Preckel D., Hanebuth D., Fischer J.E. Delayed response and lack of habituation in plasma interleukin-6 to acute mental stress in men. Brain Behav. Immun. 2006, 20:40-48.
68. Wannamethee S.G., Lowe G.D.O., Shaper A.G., Rumley A., Lennon L., Whincup P.H. Associations between cigarette smoking, pipe/cigar smoking, and smoking cessation, and haemostatic and inflammatory markers for cardiovascular disease. Eur. Heart J. 2005, 26:1765-1773.
69. Wannamethee S.G., Whincup P.H., Rumley A., Lowe G.D.O. Inter-relationships of interleukin-6, cardiovascular risk factors and the metabolic syndrome among older men. J. Thromb. Haemost. 2007, 5:1637-1643.
70. Webster J.C., Cidlowski J.A. Downregulation of the glucocorticoid receptor. A mechanism for physiological adaptation to hormones. Ann. N.Y. Acad. Sci. 1994, 746:216-220.
71. Webster J.I., Tonelli L., Sternberg E.M. Neuroendocrine regulation of immunity. Annu. Rev. Immunol. 2002, 20:125-163.