Stress and antibody response to vaccination: Implications of animal studies for human clinical research

Expert Review of Vaccines

Volumn 3, Issue 2, 2004, Pages 141-149

  Burns, Victoria E ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Animal research; Antibody response to immunization; Human research; Psychoneuroimmunology; Stress

Indexed keywords

CYCLOPHOSPHAMIDE; ENTOXANA; HEPATITIS B VACCINE; INFLUENZA VACCINE; KEYHOLE LIMPET HEMOCYANIN; MIFEPRISTONE; PNEUMOCOCCUS VACCINE;

ANTIBODY RESPONSE; HUMAN; IMMOBILIZATION STRESS; INFLUENZA VACCINATION; LOW DRUG DOSE; MENTAL STRESS; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; REVIEW; THYMUS;

ANIMALS; ANTIBODY FORMATION; HUMANS; RANDOMIZED CONTROLLED TRIALS; RESEARCH; STRESS, PSYCHOLOGICAL; VACCINATION;

EID: 1842786524     PISSN: 14760584     EISSN: None     Source Type: Journal    
DOI: 10.1586/14760584.3.2.141     Document Type: Review

References (75)

1. Kiecolt-Glaser JK, Fisher LD, Ogrocki P et al. Marital quality, marital disruption and immune function. Psychosom. Med. 49, 13-34 (1987).
2. Kiecolt-Glaser JK, Glaser R, Shuttleworth EC et al. Chronic stress and immunity in family caregivers of Alzheimer's disease victims. Psychosom. Med. 49, 523-535 (1987).
3. Futterman AD, Wellisch DK, Zighelboim J et al. Psychological and immunological reactions of family members to patients undergoing bone marrow transplantation. Psychosom. Med. 58, 472-480 (1996).
4. Schaeffer MA, McKinnon, Baum A et al. Immune status as a function of chronic stress at Three Mile Island. Psychosom. Med. 47, 85 (1985).
5. Bartrop RW, Luckhurst E, Lazarus L et al. Depressed lymphocyte function after bereavement. Lancet 1, 834-836 (1977).
6. Schleifer SJ, Keller SE, Camerino M et al. Suppression of lymphocyte stimulation following bereavement. J. Am. Med. Assoc. 250, 374-377 (1983).
7. Workman EA, La Via MF. T-lymphocyte polyclonal proliferation: effects of stress and stress response style on medical students taking National Board examinations. Clin. Immunol. Immunopathol. 43, 308-313 (1987).
8. Arnetz BB, Wasserman J, Petrini B et al. Immune function in unemployed women. Psychosom. Med. 49, 3-12 (1987).
9. Kiecolt-Glaser JK, Glaser R, Cacioppo JT et al. Marital conflict in older adults: Endocrinological and immunological correlates. Psychosom. Med. 59, 339-349 (1997).
10. Vedhara K, Fox JD, Wang ECY. The measurement of stress-related immune dysfunction in psychoneuroimmunology. Neurosci. Biobehav. Rev. 23, 699-715 (1999).
11. Cohen S, Miller GE, Rabin BS. Psychological stress and antibody response to immunization: a critical review of the human literature. Psychosom. Med. 63, 7-18 (2001). Clearly reviews the human vaccination literature.
12. Burns VE, Carroll D, Ring C, Drayson M. Antibody response to vaccination and psychosocial stress in humans: relationships and mechanisms. Vaccine 21(19-20), 2523-2534 (2003). Updates and extends the previous review of human vaccination literature.
13. Sheehy N, Chapman A, Conran W. Biographical Dictionary of Psychology. Routledge, London, UK (1997).
14. Tewes U. Concepts in Psychology. In: Psychoneuroimmunology: an Interdisciplinary Introduction. Schedlowski M, Tewes U (Eds), Plenum, London, UK, 95-111 (1999).
15. McEwen BS, Wingfield JC. The concept of allostasis in biology and biomedicine. Horm. Behav. 43(1), 2-15 (2003).
16. Martinez M, Calvo-Torrent A, Angeles Pico-Alfonso M. Social defeat and subordination as models of social stress in laboratory rodents. Aggressive Behav. 24, 241-256 (1998).
17. Shanks N, Kusnecov AW. Differential immune reactivity to stress in BALB/cByJ and C57BL/6J mice: in vivo dependence on macrophages. Physiol. Behav. 65(1), 95-103 (1998).
18. Snyder BK, Roghmann KJ, Sigal LH. Effect of stress and other biopsychosocial factors on primary antibody response. J. Adolesc. Health 11, 472-479 (1990).
19. Glaser R, Kiecolt-Glaser JK, Bonneau RH et al. Stress-induced modulation of the immune response to recombinant hepatitis B vaccine. Psychosom. Med. 54, 22-29 (1992).
20. Smith A, Vollmer-Conna U, Bennett B et al. The relationship between distress and the development of a primary immune response to a novel antigen. Brain Behav. Immun. 18(1), 65-75 (2004).
21. Burns VE, Carroll D, Ring C et al. Stress, coping and hepatitis B antibody status. Psychosom. Med. 64, 287-293 (2002).
22. Jabaaij L, Grosheide PM, Heijtink RA et al. Influence of perceived psychological stress and distress on antibody response to low dose rDNA hepatitis B vaccine. J. Psychosom. Res. 37, 361-369 (1993).
23. Jabaaij L, van Hattum J, Vulgerhoets JJM et al. Modulation of immune response to rDNA hepatitis B vaccination by psychological stress. J. Psychosom. Res. 41, 129-137 (1996).
24. Marsland AL, Cohen S, Rabin BS, Manuck SB. Associations between stress, trait negative affect, acute immune reactivity and antibody response to hepatitis B injection in healthy young adults. Health Psychol. 20, 4-11 (2001).
25. Petry J, Weems LB, Livingstone JN. Relationship of stress, distress and the immunologic response to a recombinant hepatitis B vaccine. J. Fam. Pract. 32, 481-486 (1991).
26. Patriarca PA. A randomized controlled trial of influenza vaccine in the elderly: scientific scrutiny and ethical responsibility. J. Am. Med. Assoc. 272, 1700-1701 (1994).
27. Wallsten SM. Comparing patterns of stress in daily experiences of elderly caregivers and non-caregivers. Int. J. Aging Hum. Dev. 37, 55-68 (1993).
28. Kiecolt-Glaser JK, Glaser R, Gravenstein S et al. Chronic stress alters the immune response to influenza virus vaccine in older adults. Proc. Natl Acad. Sci. USA 93, 3043-3047 (1996).
29. Vedhara K, Cox NKM, Wilcock GK et al. Chronic stress in elderly carers of dementia patients and antibody response to influenza vaccination. Lancet 353, 627-631 (1999). Shows the impact of caregiving on antibody response to vaccination and the relationship with cortisol.
30. Glaser R, Kiecolt-Glaser JK, Malarkey W, Sheridan JF. The influence of psychological stress on the immune response to vaccines. Ann. NY Acad. Sci. 840, 649-655 (1998). Provides an overview of the caregiver studies.
31. Vedhara K, McDermott MP, Evans TG et al. Chronic stress in nonelderly caregivers: psychological, endocrine and immune implications. J. Psychosom. Res. 53, 1153-1161 (2002).
32. Kohut ML, Cooper MM, Nickolaus MS et al. Exercise and psychosocial factors modulate immunity to influenza vaccine in elderly individuals. J. Gerontol. Med. Sci. 57A, M557-M562 (2002).
33. Larson MR, Treanor JJ, Ader R. Psychosocial influences on responses to reduced and full-dose trivalent inactivated influenza vaccine. Psychosom. Med. 64, 113 (2002).
34. Pressman S, Cohen S, Miller G, Rabin B. Stress and antibody response to immunization in college freshman. Brain, Behav. Immun. 16, 208 (2002).
35. Burns VE, Carroll D, Drayson M et al. Life events, perceived stress and antibody response to influenza vaccination in young, healthy adults. J. Psychosom. Res. 55, 569-572 (2003).
36. Boyce WT, Adams S, Tschann JM et al. Adrenocortical and behavioral predictors of immune response to starting school. Pediatr. Res. 38, 1009-1016 (1995).
37. Glaser R, Sheridan JF, Malarkey W et al. Chronic stress modulates the immune response to a pneumococcal pneumonia vaccine. Psychosom. Med. 62, 804-807 (2000). Demonstrate the effects of stress on a thymus-independent antibody response to vaccination in humans.
38. Burns VE, Drayson M, Ring C, Carroll D. Perceived stress and psychological wellbeing are associated with antibody status after meningitis C conjugate vaccination. Psychosom. Med. 64(6), 963-970 (2002). Demonstrate the effect of stress on antibody response to a conjugate vaccination in humans.
39. Morag M, Morag A, Reichenberg A et al. Psychological variables as predictors of rubella antibody titers and fatigue - a prospective double-blind study. J. Psychiatr. Res. 33, 389-395 (1999).
40. Shanks N, Griffiths J, Zalcman S et al. Mouse strain differences in plasma corticosterone following uncontrollable footshock. Pharmacol. Biochem. Behav. 36(3), 515-519 (1990).
41. Shanks N, Zalcman S, Zacharko RM, Anisman H. Alterations of central noradrenaline, dopamine and serotonin in several strains of mice following acute stressor exposure. Pharmacol. Biochem. Behav. 38(1), 69-75 (1991).
42. Shanks N, Anisman H. Stressor-provoked behavioral changes in six strains of mice. Behav. Neurosci. 102(6), 894-905 (1988).
43. Burns VE, Ring C, Drayson M, Carroll D. Cortisol and cardiovascular reactions to mental stress and antibody status following hepatitis B vaccination: A preliminary study. Psychophysiology 39, 361-368 (2002). Examines the role of reactivity in antibody response to vaccination in humans.
44. Karp JD, Moynihan JA, Ader R. Effects of differential housing on the primary and secondary antibody responses of male C57BL/6 and BALB/c mice. Brain Behav. Immun. 7(4), 326-333 (1993).
45. Zalcman S, Richter M, Anisman H. Alterations of immune functioning following exposure to stressor-related cues. Brain Behav. Immun. 3(2), 99-109 (1989).
46. Zalcman S, Anisman H. Acute and chronic stressor effects on the antibody response to sheep red blood cells. Pharmacol. Biochem. Behav. 46(2), 445-452 (1993). Demonstrates the complex interaction between acute stress exposures and antibody response in an animal model.
47. Zalcman S, Richter M, Anisman H. Alterations of immune functioning following exposure to stressor-related cues. Brain Behav. Immun. 3(2), 99-109 (1989).
48. Carroll D, Davey Smith G, Bennett P. Some observations on health and socioeconomic status. J. Health Psychol. 1(1), 23-39 (2003).
49. Fleshner M, Laudenslager ML, Simons L, Maier SF. Reduced serum antibodies associated with social defeat in rats. Physiol. Behav. 45, 1183-1187 (1989).
50. Bartolomucci A, Sacerdote P, Panerai AE et al. Chronic psychosocial stress-induced downregulation of immunity depends upon individual factors. J. Neuroimmunol. 141(1-2), 58-64 (2003).
51. Evans P, Der G, Ford G et al. Social class, sex and age differences in mucosal immunity in a large community sample. Brain Behav. Immun. 14(1), 41-48 (2000).
52. Petrie KJ, Booth RJ, Pennebaker JW et al. Disclosure of trauma and immune response to a hepatitis B vaccination program. J. Consult. Clin. Psychol. 63, 787-792 (1995).
53. Vedhara K, Bennett PD, Clark S et al. Enhancement of antibody responses to influenza vaccination in the elderly following a cognitive-behavioral stress management intervention. Psychother. Psychosom. 72(5), 245-252 (2003).
54. Davidson RJ, Kabat-Zinn J, Schumacher J et al. Alterations in brain and immune function produced by mindfulness meditation. Psychosom. Med. 65(4), 564-570 (2003).
55. Moher D, Pham B, Jones A et al. Does quality of reports of randomized trials affect estimates of intervention efficacy reported in meta-analyses? Lancet 352, 609-613 (1998).
56. Lange T, Perras B, Fehm HL, Born J. Sleep enhances the human antibody response to hepatitis A vaccination. Psychosom. Med. 65(5), 831-835 (2003).
57. Fleshner M. Exercise and neuroendocrine regulation of antibody production: protective effect of physical activity on stress-induced suppression of the specific antibody response. Int. J. Sports Med. 21(Suppl. 1), S14-S19 (2000). Demonstrates the possible protective role of exercise.
58. Moraska A, Fleshner M. Voluntary physical activity prevents stress-induced behavioral depression and anti-KLH antibody suppression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281(2), 484-489 (2001).
59. Dhabhar FS. Stress-induced augmentation of immune function - the role of stress hormones, leukocyte trafficking and cytokines. Brain Behav. Immun. 16, 785-798 (2002). Reviews the possible beneficial effects of acute stress on antibody response to vaccination.
60. Wood PG, Karol MH, Kusnecov AW, Rabin BS. Enhancement of antigen-specific humoral and cell-mediated immunity by electric footshock stress in rats. Brain Behav. Immun. 7(2), 121-34 (1993).
61. Silberman DM, Wald MR, Genaro AM. Acute and chronic stress exert opposing effects on antibody responses associated with changes in stress hormone regulation of T-lymphocyte reactivity. J. Neuroimmunol. 144(1-2), 53-60 (2003).
62. Solomon GF. Stress and antibody response in rats. Intern. Arch. Allergy 35, 97-104 (1969).
63. Karp JD, Smith J, Hawk K. Restraint stress augments antibody production in cyclophosphamide-treated mice. Physiol. Behav. 70(3-4), 271-278 (2000).
64. Moynihan JA, Ader R, Grota Lj et al. The effects of stress on the development of immunological memory following low-dose antigen priming in mice. Brain Behav. Immun. 4(1), 1-12 (1990).
65. Feng N, Pagniano R, Tovar CA et al. The effect of restraint stress on the kinetics, magnitude and isotype of the humoral immune response to influenza virus infection. Brain Behav. Immun. 5(4), 370-382 (1991).
66. Fleshner M, Brennan FX, Nguyen K et al. RU-486 blocks differentially suppressive effect of stress on in vivo anti-KLH immunoglobulin response. Am. J. Physiol. 271, R1344-R1352 (1996). Provides insight into the possible role of cortisol as a mediator of this relationship.
67. Esterling BA, Rabin BS. Stress-induced alteration of T-lymphocyte subsets and humoral immunity in mice. Behav. Neurosci. 101, 115-119 (1987).
68. Fleshner M, Deak T, Nguyen KT et al. Endogenous glucocorticoids play a positive regulatory role in the antikeyhole limpet hemocyanin in vivo antibody response. J. Immunol. 166(6), 3813-3819 (2001).
69. Moraska A, Campisi J, Nguyen KT et al. Elevated IL-1β contributes to antibody suppression produced by stress. J. Appl. Physiol. 93(1), 207-215 (2002).
70. Costanzo ES, Lutgendorf SK, Kohut ML et al. Mood and cytokine responses to influenza. 16(2), 177-178 (2002).
71. Cohen J. Things I have learned (so far). Am. Psychol. 45, 1304-1312 (1990).
72. Sacerdote P, Manfredi B, Gaspani L, Panerai AE. The opioid antagonist naloxone induces a shift from Type 2 to Type 1 cytokine pattern in BALB/cJ mice. Blood 95(6), 2031-2036 (2000).
73. Sanders VM, Straub RH. Noradrenaline, the β-adrenergic receptor and immunity. Brain Behav. Immun. 16(4), 290-332 (2001).
74. Murray SE, Lallman HR, Heard AD et al. A genetic model of stress displays decreased lymphocytes and impaired antibody responses without altered susceptibility to Streptococcus pneumoniae. J. Immunol. 167, 691-698 (2001).
75. Glaser R, Robles TF, Sheridan J et al. Mild depressive symptoms are associated with amplified and prolonged inflammatory responses after influenza virus vaccination in older adults. Arch. Gen. Psychiatry 60(10), 1009-1014 (2003).