Sleep and antibody response to hepatitis B vaccination.

STUDY OBJECTIVES Experimental evidence links poor sleep with susceptibility to infectious illness; however, it remains to be determined if naturally occurring sleep is associated with immune responses known to play a role in protection against infection. The aim of this study was to determine whether sleep duration, sleep efficiency, and sleep quality, assessed in the natural environment, predict magnitude of antibody responses to a novel antigen among community volunteers in midlife. DESIGN Observational. MEASUREMENTS AND RESULTS Healthy midlife adults (n = 125; 70 female; age 40-60 yr) received the standard 3-dose hepatitis B vaccination series. Actigraphy and electronic sleep diaries were used to assess sleep duration, sleep efficiency, and subjective sleep quality. Viral-specific antibody titers were obtained prior to the 2nd and 3rd vaccination to assess primary and secondary antibody responses. Clinical protection status (anti-hepatitis B surface antigen immunoglobulin G ≥ 10 mIU/ml) was assessed 6 mo after the final immunization. Regression analyses revealed that shorter actigraphy-based sleep duration was associated with a lower secondary antibody response independent of age, sex, body mass index, and response to the initial immunization. Shorter sleep duration, measured by actigraphy and sleep diary, also predicted a decreased likelihood of being clinically protected from hepatitis B at the conclusion of the vaccination series. Neither sleep efficiency nor subjective sleep quality were significant predictors of antibody response. CONCLUSIONS Short sleep duration in the natural environment may negatively affect in vivo antibody responses to novel antigens, providing a possible explanation for observed associations of poor sleep with increased susceptibility to infectious disease.

[1]  William J Doyle,et al.  Sleep habits and susceptibility to the common cold. , 2009, Archives of internal medicine.

[2]  Nicholas W. Kin,et al.  It takes nerve to tell T and B cells what to do , 2006, Journal of leukocyte biology.

[3]  P. Meerlo,et al.  Restricted and disrupted sleep: effects on autonomic function, neuroendocrine stress systems and stress responsivity. , 2008, Sleep medicine reviews.

[4]  L. Gallicchio,et al.  Sleep duration and mortality: a systematic review and meta‐analysis , 2009, Journal of sleep research.

[5]  Jan Born,et al.  Sleep Enhances the Human Antibody Response to Hepatitis A Vaccination , 2003, Psychosomatic medicine.

[6]  Atul Malhotra,et al.  A prospective study of sleep duration and coronary heart disease in women. , 2003, Archives of internal medicine.

[7]  J. Born,et al.  Sleep after Vaccination Boosts Immunological Memory , 2011, The Journal of Immunology.

[8]  D. Bovbjerg,et al.  Psychological stress and antibody response to influenza vaccination: A meta-analysis , 2009, Brain, Behavior, and Immunity.

[9]  John Trinder,et al.  Sick and tired: does sleep have a vital role in the immune system? , 2004, Nature Reviews Immunology.

[10]  D. Kripke,et al.  Mortality associated with sleep duration and insomnia. , 2002, Archives of general psychiatry.

[11]  J. Manson,et al.  A prospective study of self-reported sleep duration and incident diabetes in women. , 2003, Diabetes care.

[12]  Leads from the MMWR. Recommendations of the immunization practices advisory committee update on hepatitis B prevention. , 1987, JAMA.

[13]  C. Pollak,et al.  The role of actigraphy in the study of sleep and circadian rhythms. , 2003, Sleep.

[14]  W. Malarkey,et al.  Stress‐induced modulation of the immune response to recombinant hepatitis B vaccine. , 1992, Psychosomatic medicine.

[15]  J. Hadler,et al.  Hepatitis B vaccine responsiveness in Connecticut public safety personnel. , 1993, JAMA.

[16]  Kenneth P. Wright,et al.  The effects of 40 hours of total sleep deprivation on inflammatory markers in healthy young adults , 2007, Brain, Behavior, and Immunity.

[17]  E. van Cauter,et al.  Effect of sleep deprivation on response to immunization. , 2002, JAMA.

[18]  C. Guilleminault,et al.  Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. , 2004, Sleep.

[19]  C. Ring,et al.  Antibody response to vaccination and psychosocial stress in humans: relationships and mechanisms. , 2003, Vaccine.

[20]  J. Born,et al.  Number and function of circulating human antigen presenting cells regulated by sleep. , 2007, Sleep.

[21]  Nader Rifai,et al.  Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk. , 2004, Journal of the American College of Cardiology.

[22]  C. Ring,et al.  Acute stress exposure prior to influenza vaccination enhances antibody response in women , 2006, Brain, Behavior, and Immunity.

[23]  Stoyan Dimitrov,et al.  Effects of sleep and circadian rhythm on the human immune system , 2010, Annals of the New York Academy of Sciences.

[24]  N. Kawakami,et al.  Coemergence of Insomnia and a Shift in the Th1/Th2 Balance toward Th2 Dominance , 2003, Neuroimmunomodulation.

[25]  J. Zuckerman Protective efficacy, immunotherapeutic potential, and safety of hepatitis B vaccines , 2006, Journal of medical virology.

[26]  F. Romão,et al.  Changes in the immune system during menopause and aging. , 2010, Frontiers in bioscience.

[27]  J. Born,et al.  Sleep associated regulation of T helper 1/T helper 2 cytokine balance in humans , 2004, Brain, Behavior, and Immunity.

[28]  J. Broman,et al.  Sleep complaints predict coronary artery disease mortality in males: a 12‐year follow‐up study of a middle‐aged Swedish population , 2002, Journal of internal medicine.

[29]  Stoyan Dimitrov,et al.  Cortisol and epinephrine control opposing circadian rhythms in T cell subsets. , 2009, Blood.

[30]  E. Bixler,et al.  Adverse effects of modest sleep restriction on sleepiness, performance, and inflammatory cytokines. , 2004, The Journal of clinical endocrinology and metabolism.

[31]  John J. Treanor,et al.  Psychological Stress and Antibody Response to Influenza Vaccination: When Is the Critical Period for Stress, and How Does It Get Inside the Body? , 2004, Psychosomatic medicine.

[32]  J. L. Yeh,et al.  Subjective and Objective Sleep Quality and Aging in the Sleep Heart Health Study , 2008, Journal of the American Geriatrics Society.

[33]  Andrew G Rundle,et al.  Sleep duration as a risk factor for diabetes incidence in a large U.S. sample. , 2007, Sleep.

[34]  J. Born,et al.  Cytokine production and lymphocyte subpopulations in aged humans. An assessment during nocturnal sleep , 1995, Mechanisms of Ageing and Development.

[35]  1983 metropolitan height and weight tables. , 1983, Statistical bulletin.

[36]  J. Kruppenbacher,et al.  Immunogenicity of a Recombinant Hepatitis B Vaccine in Adults , 1996 .

[37]  D. Muller,et al.  Humoral Immune Responses to Influenza Vaccination in Patients with Obstructive Sleep Apnea , 2007, Pharmacotherapy.

[38]  M. Osterholm,et al.  Risk factors for lack of detectable antibody following hepatitis B vaccination of Minnesota health care workers. , 1993, JAMA.

[39]  J. Mullington,et al.  Elevated inflammatory markers in response to prolonged sleep restriction are associated with increased pain experience in healthy volunteers. , 2007, Sleep.

[40]  H. Schiöth,et al.  Acute sleep deprivation has no lasting effects on the human antibody titer response following a novel influenza A H1N1 virus vaccination , 2012, BMC Immunology.

[41]  F. Hu,et al.  A prospective study of sleep duration and pneumonia risk in women. , 2012, Sleep.

[42]  M. Irwin,et al.  Partial night sleep deprivation reduces natural killer and celhdar immune responses in humans , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[43]  H. Moldofsky,et al.  Effects of sleep deprivation on human immune functions , 1989, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[44]  C. Grossman Regulation of the immune system by sex steroids. , 1984, Endocrine reviews.

[45]  T. Smith,et al.  Partial sleep deprivation reduces natural killer cell activity in humans. , 1994, Psychosomatic medicine.

[46]  J. Sheridan,et al.  Effect of Sleep Deprivation on Response to Immunizaton , 2002 .

[47]  E. van Cauter,et al.  Impact of Sleep and Its Disturbances on Hypothalamo-Pituitary-Adrenal Axis Activity , 2010, International journal of endocrinology.

[48]  Sheldon Cohen,et al.  Psychological Stress and Antibody Response to Immunization: A Critical Review of the Human Literature , 2001, Psychosomatic medicine.

[49]  M. Guillard,et al.  Effect of one night of sleep loss on changes in tumor necrosis factor alpha (TNF-α) levels in healthy men. , 2011, Cytokine.

[50]  T. Kamarck,et al.  A global measure of perceived stress. , 1983, Journal of health and social behavior.

[51]  J. Born,et al.  Effects of sleep and circadian rhythm on human circulating immune cells. , 1997, Journal of immunology.

[52]  Max Hirshkowitz,et al.  Practice parameters for the role of actigraphy in the study of sleep and circadian rhythms: an update for 2002. , 2003, Sleep.

[53]  D. Cardinali,et al.  Melatonin and the Immune System in Aging , 2008, Neuroimmunomodulation.

[54]  Pauline Heslop,et al.  Sleep duration and mortality: The effect of short or long sleep duration on cardiovascular and all-cause mortality in working men and women. , 2002, Sleep medicine.

[55]  M. Irwin,et al.  Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. , 2006, Archives of internal medicine.

[56]  F. Cappuccio,et al.  Sleep duration and all-cause mortality: a systematic review and meta-analysis of prospective studies. , 2010, Sleep.

[57]  W. Solbach,et al.  Sleep‐dependent activity of T cells and regulatory T cells , 2009, Clinical and experimental immunology.

[58]  M. Marmot,et al.  Gender differences in the cross-sectional relationships between sleep duration and markers of inflammation: Whitehall II study. , 2009, Sleep.

[59]  J. Mullington,et al.  Sleep loss and inflammation. , 2010, Best practice & research. Clinical endocrinology & metabolism.

[60]  A. Schwartz,et al.  Adult obstructive sleep apnea: pathophysiology and diagnosis. , 2007, Chest.

[61]  C. Meisinger,et al.  Sleep duration and sleep complaints and risk of myocardial infarction in middle-aged men and women from the general population: the MONICA/KORA Augsburg cohort study. , 2007, Sleep.

[62]  H. Margolis,et al.  Immunogenicity of hepatitis B Vaccines. Implications for persons at occupational risk of hepatitis B virus infection. , 1998, American journal of preventive medicine.