Bereavement and marriage are associated with antibody response to influenza vaccination in the elderly

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Abstract

Stressful life events exposure including bereavement, an event commonly experienced by elderly people, social support, marital status, and satisfaction were examined in relation to antibody response to the annual trivalent influenza vaccination in an elderly community sample (N = 184). Antibody response was assessed at baseline, and at 1 and 12 months following vaccination. Taking into account baseline antibody titer, overall life events exposure and social support were not associated with response to any of the influenza strains. However, bereavement in the year prior to vaccination was negatively associated with the 1-month response to the A/Panama and B/Shangdong strains. Being married and having higher marital satisfaction was also associated with higher peak responses to the A/Panama influenza strain at 1 month. The positive association between marital satisfaction and A/Panama response was particularly evident in the younger half of the married sample. These associations largely withstood adjustment for potential confounders. Thus, in the elderly, peak antibody response was associated with bereavement and marriage, and not the more general factors, life events and social support, related to antibody response in student samples. This suggests the importance of taking a life course approach to examining relationships between psychosocial factors and immunity, and that interventions to modify the impact of these factors should address those most salient for each age group.

Introduction

The antibody response to vaccination is considered a useful means of studying psychosocial influences on in vivo immune function (Burns et al., 2003b, Cohen et al., 2001, Vedhara et al., 1999b). The most consistent finding is the association between frequent exposure to stressful life events and/or high levels of perceived stress and a poorer antibody response to a variety of vaccinations (Burns et al., 2003b, Cohen et al., 2001, Glaser et al., 1992, Glaser et al., 1998, Glaser et al., 2000, Kiecolt-Glaser et al., 1996, Kohut et al., 2002, Miller et al., 2004, Phillips et al., 2005a, Vedhara et al., 1999a, Yang and Glaser, 2002). The majority of this research has been carried out in younger samples. Most of the studies in older populations have used the caregiver-control model, in which the vaccination response of elderly people care-giving for a spouse with dementia are compared to those of non-care-giving controls. These studies have demonstrated that exposure to this very severe life stressor is associated with poor antibody responses to both influenza (Glaser et al., 1998, Glaser et al., 2000, Kiecolt-Glaser et al., 1996, Vedhara et al., 1999a) and pneumococcal (Glaser et al., 2000) vaccinations. Whether this effect is generalisable to elderly individuals experiencing a range of more mundane stress exposures remains unclear. Although one study has reported that perceived stress was associated with a poorer antibody response to the influenza vaccine in the elderly (Kohut et al., 2002), a recent small scale study found no association between perceived stress and antibody status following this vaccination in elderly nursing home residents (Moynihan et al., 2004). There are no published studies to date on the association between stressful life events exposure and vaccination response in the elderly. In particular, given the likelihood of exposure to bereavement in the elderly, and the negative and long-term impact it has (Bodnar and Kiecolt-Glaser, 1994), this specific life event is also worth studying in this context, especially as bereavement has been negatively related to natural killer cell cytotoxicity and lymphocyte proliferation to mitogen (Bartrop et al., 1977, Goodkin et al., 1996, Irwin et al., 1987, Kemeny et al., 1995, Schleifer et al., 1983, Zisook et al., 1994).

Psychosocial factors other than psychological stress have received less attention in the context of the vaccination model, particularly in the elderly. The relationship between social support and the antibody response has been examined in three studies of student samples. First, greater social support was associated with a stronger combined immune response to the booster third inoculation of the hepatitis B vaccination (Glaser et al., 1992). Second, loneliness and smaller social network size were related to a poorer antibody response to the A/New Caledonian strain of the influenza vaccination (Pressman et al., 2005). Third, better social support was associated with stronger antibody responses to the A/Panama strain following influenza vaccination (Phillips et al., 2005a). In contrast, in the only study of social support in the elderly, social support was negatively correlated with A/Panama influenza strain antibody status following vaccination (Moynihan et al., 2004). Further examination of the association between social support in the elderly and the antibody response is warranted.

There is also evidence that marriage is beneficial to health; unmarried individuals suffer greater morbidity and mortality from a range of acute and chronic conditions (Gordon and Rosenthal, 1995, House et al., 1988, Verbrugge, 1979). However, it is not only marital status which has been found to be associated with psychological and physical health, but also the quality of marriage (see e.g., Kiecolt-Glaser and Newton, 2001, Robles and Kiecolt-Glaser, 2003). There is growing evidence that marital quality relates to immune function. Using in vitro immune measures, individuals reporting poorer marital quality displayed higher Epstein–Barr virus titers, indicating poorer latent virus control, and a poorer blastogenic response to PHA mitogen (Kiecolt-Glaser et al., 1987, Kiecolt-Glaser et al., 1988). Marital conflict has also been found to be associated with poorer natural killer cell lysis (Miller et al., 1999), poorer blastogenic response to two mitogens, and increased Epstein–Barr virus titers (Kiecolt-Glaser et al., 1993, Kiecolt-Glaser et al., 1997). As far as we are aware, marital status and satisfaction has not yet been assessed in relation to antibody status following vaccination.

The present study exploited the UK National Health Service initiative to immunize annually persons over the age of 65 years with the trivalent influenza vaccination. The association between life events exposure in general, and bereavement in particular, social support, marital status and satisfaction, and the antibody response to the vaccination was examined in a sample of those taking part in this programme. It was hypothesized that participants with higher life events exposure, and lower social support would exhibit lower antibody titers following vaccination. It was also hypothesized that individuals who were married and especially those with high marital satisfaction would also show a better antibody response to the vaccine.

Section snippets

Participants

One hundred and eighty-four elderly people (80 men and 104 women) were recruited from five medical practices in Birmingham, UK between September and November 2003. All participants were aged 65 years or older and had no history of negative reactions to blood sampling, no acute infection, or known current immune disorder. Baseline demographic information was provided by 154 participants. Participants’ mean age at entry to the study was 74.6 (SD = 6.26) years and their mean body mass index, based

Questionnaire data

The median (interquartile range) number of life events was 2 (4). The mean (SD) life events score, weighted for self-rated severity, was 16.7 (21.30). Forty-five (32%) participants had suffered bereavement in the year prior to vaccination; of these 45, only seven had experienced spousal bereavement. The mean (SD) number of close friends was 7.3 (6.50), and total functional social support score was 74.2 (17.04). Sixty-six (63%) of the participants sampled were married/cohabiting, and their mean (SD)

Discussion

Participants’ overall stressful life events exposure was not significantly associated with the antibody response to influenza vaccination. However, one particular life event, bereavement, was negatively associated with 1-month antibody titer against the A/Panama and B/Shangdong strains. In addition, although social network size and functional social support were not related to antibody response, married/cohabiting participants showed a better antibody response to the A/Panama strain at 1 month

Acknowledgments

The authors acknowledge the invaluable help of the MidRec Research Practices Consortium for providing financial and organisational assistance; the Bellevue, Greenridge, Griffins Brook, West Heath, and Woodgate Valley GP surgeries in Birmingham, UK, for their accommodation and facilitation of blood collection; Ms. Kate Edwards for help with blood sampling; Ms. Jenny Clapham and Ms. Vicky Crispin for help with recruitment and data entry; and finally Ms. Meghann Mason, Ms. Michelle Sharpe, and Mr.

References (53)

  • C.D. Sherbourne et al.

    The MOS social support survey

    Soc. Sci. Med.

    (1991)
  • K. Vedhara et al.

    Chronic stress in elderly carers of dementia patients and antibody response to influenza vaccination

    Lancet

    (1999)
  • K. Vedhara et al.

    The measurement of stress-related immune dysfunction in psychoneuroimmunology

    Neurosci. Biobehav. Rev.

    (1999)
  • S. Zisook et al.

    Bereavement, depression, and immune function

    Psychiatr. Res.

    (1994)
  • L.S. Aiken et al.

    Multiple Regression: Testing and Interpreting Interactions

    (1991)
  • J.C. Bodnar et al.

    Caregiver depression after bereavement: chronic stress isn’t over when it’s over

    Psychol. Aging

    (1994)
  • A. Bowling

    Mortality after bereavement: an analysis of mortality rates and associations with mortality thirteen years after bereavement

    Int. J. Geriatr. Psychiatr.

    (1994)
  • G.W. Brown et al.

    Social Origins of Depression: A Study of Psychiatric Disorder in Women

    (1989)
  • D. Carroll et al.

    Life events and hemodynamic stress reactivity in the middle-aged and elderly

    Psychophysiology

    (2005)
  • N.J. Christenfeld et al.

    Risk factors, confounding, and the illusion of statistical control

    Psychosom. Med.

    (2004)
  • S. Cohen et al.

    Psychological stress and antibody response to immunization: a critical review of the human literature

    Psychosom. Med.

    (2001)
  • J.C. Coyne et al.

    Going beyond social support: the role of social relationships in adaptation

    J. Consult. Clin. Psychol.

    (1986)
  • M.H. Freeston et al.

    Reconsideration of the Locke-Wallace marital adjustment test: is it still relevant for the 1990s?

    Psychol. Rep.

    (1997)
  • R. Glaser et al.

    Stress-induced modulation of the immune response to recombinant hepatitis B vaccine

    Psychosom. Med.

    (1992)
  • R. Glaser et al.

    The influence of psychological stress on the immune response to vaccines

    Ann. N.Y. Acad. Sci.

    (1998)
  • R. Glaser et al.

    Chronic stress modulates the immune response to a pneumococcal pneumonia vaccine

    Psychosom. Med.

    (2000)
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