Healthy Smoker: An Oxymoron? Maybe, But It Is More Complicated Than That

  • Jeanette M. Bennett
  • Lydia G. Roos
  • Joseph S. Marino
  • Nicolas Rohleder
  • Maren J. Coffman


Tobacco use reliably increases the likelihood of chronic disease development and premature death. However, the initiation of tobacco use does not immediately result in clinical disease manifestation. We recruited 24 healthy smokers and 24 age-, sex-, and BMI-matched never smokers to examine changes in immune function prior to clinical disease manifestations (e.g., no diagnosis or drug treatment for chronic health conditions). In addition to immune cell reactivity to lipopolysaccharide (LPS) and dexamethasone (DEX), we collected psychosocial and physical and mental health data. Smokers were moderately addicted to nicotine and had been smoking for an average of 6.6 years (standard error of mean [SEM] = 1.4) and had 9.4 pack years (SEM 1.9) of tobacco exposure. Smokers endorsed poorer sleep as well as greater psychological distress including anxiety, depression, and loneliness, compared to never smokers. In addition, smokers’ immune cells were less reactive to LPS than never smokers’. Thus, smokers exhibit poorer mental and physical health and modulation of their immune response compared to never smokers, indicating that the term “healthy smoker” is an oxymoron. However, the reduction of immune function observed in smokers was also found in never smokers who had higher levels of loneliness. Hence, loneliness may be as immuno-dysregulating as smoking. Upon further investigation, replacing smoking status with self-rated health explained more of the variability in immune cell responses. Overall, these findings caution the use of one facet, like smoking, as a definitive factor driving health status. When determining global health functioning, we must factor in as many facets as possible, as a long-term or trait-like negative emotion can be just a “unhealthy” as a negative health behavior. In this sample, individuals appear to be aware of their “healthiness,” and it was linked to immune dysregulation.



All work was supported by internal funds awarded via competitive opportunities within the University of North Carolina at Charlotte including the Faculty Research Grants, ARCHES, and the Department of Psychological Science. We thank the dedicated assistance of past and present StressWAVES BRL research assistants who supported the data collection for this project.


  1. 1.
    Guyer B, Freedman MA, Strobino DM, Sondik EJ. Annual summary of vital statistics: trends in the health of Americans during the 20th century. Pediatrics. 2000;106(6):1307–17.Google Scholar
  2. 2.
    Kiecolt-Glaser JK, Wilson SJ. Psychiatric disorders, morbidity, and mortality: tracing mechanistic pathways to accelerated aging. Psychosom Med. 2016;78(7):772–5.Google Scholar
  3. 3.
    Glaser R, Kiecolt-Glaser JK. Stress-induced immune dysfunction: implications for health. Nat Rev Immunol. 2005;5:243–51.Google Scholar
  4. 4.
    Dickerson SS, Kemeny ME. Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull. 2004;130(3):355–91.Google Scholar
  5. 5.
    McEwen BS, Gianaros PJ. Central role of the brain in stress and adaptation: links to socioeconomic status, health, and disease. In: Adler NE, Stewart J, editors. Biology of disadvantage: socioeconomic status and health, vol. 1186. Malden: Wiley; 2010. p. 190–222.Google Scholar
  6. 6.
    Sapolsky RM. Stress and the brain: individual variability and the inverted-U. Nat Neurosci. 2015;18(10):1344–6.Google Scholar
  7. 7.
    McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007;87(3):873–904.Google Scholar
  8. 8.
    Thayer JF, Lane RD. A model of neurovisceral integration in emotion regulation and dysregulation. J Affect Disord. 2000;61(3):201–16.Google Scholar
  9. 9.
    Sturmberg JP, Bennett JM, Picard M, Seely AJ. The trajectory of life. Decreasing physiological network complexity through changing fractal patterns. Front Physiol. 2015;6:169.Google Scholar
  10. 10.
    Heng HHQ, Liu G, Stevens JB, Bremer SW, Ye KJ, Abdallah BY, Horne SD, Ye CJ. Decoding the genome beyond sequencing: the new phase of genomic research. Genomics. 2011;98(4):242–52.Google Scholar
  11. 11.
    Miller G, Cohen S, Ritchey A. Chronic psychological stress and the regulation of pro-inflammatory cytokines: a glucocorticoid-resistance model. Health Psychol. 2002;21(6):531–41.Google Scholar
  12. 12.
    Cohen S, Janicki-Deverts D, Doyle WJ, et al. Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proc Natl Acad Sci. 2012;109(16):5995–9.Google Scholar
  13. 13.
    Maltese P, Palma L, Sfara C, et al. Glucocorticoid resistance in Crohn’s disease and ulcerative colitis: an association study investigating GR and FKBP5 gene polymorphisms. Pharmacogenomics J. 2012;12(5):432–8.Google Scholar
  14. 14.
    Yang N, Ray DW, Matthews LC. Current concepts in glucocorticoid resistance. Steroids. 2012;77(11):1041–9.Google Scholar
  15. 15.
    Jaremka LM, Fagundes CP, Glaser R, Bennett JM, Malarkey WB, Kiecolt-Glaser JK. Loneliness predicts pain, depression, and fatigue: understanding the role of immune dysregulation. Psychoneuroendocrinology. 2013;38(8):1310–7.Google Scholar
  16. 16.
    Jaremka LM, Fagundes CP, Peng J, et al. Loneliness promotes inflammation during acute stress. Psychol Sci. 2013;24(7):1089–97.Google Scholar
  17. 17.
    Fagundes CP, Bennett JM, Alfano CM, et al. Social support and socioeconomic status interact to predict epstein-barr virus latency in women awaiting diagnosis or newly diagnosed with breast cancer. Health Psychol. 2012;31(1):11–9.Google Scholar
  18. 18.
    Bernaards CM, Twisk JWR, Snel J, Van Mechelen W, Kemper HCG. Is calculating pack-years retrospectively a valid method to estimate life-time tobacco smoking? A comparison between prospectively calculated pack-years and retrospectively calculated pack-years. Addiction. 2001;96(11):1653–61.Google Scholar
  19. 19.
    Adamopoulos D, Van De Borne P, Argacha JF. New insights into the sympathetic, endothelial and coronary effects of nicotine. Clin Exp Pharmacol Physiol. 2008;35(4):458–63.Google Scholar
  20. 20.
    Bennett JM, Marino JS, Peck B, Roos LG, Joseph KM, Carter LB, et al. Smokers display reduced glucocorticoid sensitivity prior to symptomatic chronic disease development. Ann Behav Med. 2018; Advanced publication online.
  21. 21.
    Bennett JM, Marino JS, Canevello AB, Roos LG, Coffman MJ, Rohleder N. Loneliness analogous to smoking? Lonely never smokers and smokers exhibit similar immune dysregulation. 2018; (under review).Google Scholar
  22. 22.
    Stenholm S, Kivimäki M, Jylhä M, Kawachi I, Westerlund H, Pentti J, Goldberg M, Zins M, Vahtera J. Trajectories of self-rated health in the last 15 years of life by cause of death. Eur J Epidemiol. 2016;31(2):177–85.Google Scholar
  23. 23.
    Mavaddat N, Parker RA, Sanderson S, Mant J, Kinmonth AL. Relationship of self-rated health with fatal and non-fatal outcomes in cardiovascular disease: a systematic review and meta-analysis. PLoS One. 2014;9(7):e103509.Google Scholar
  24. 24.
    Wu S, Wang R, Zhao Y, Ma X, Wu M, Yan X, He J. The relationship between self-rated health and objective health status: a population-based study. BMC Public Health. 2013;13(1):320.Google Scholar
  25. 25.
    Picard M, Juster R, Sabiston C. Is the whole greater than the sum of the parts? Self-rated health and transdisciplinarity. Health Aff. 2013;5(12A):24–30.Google Scholar
  26. 26.
    Heatherton TF, Kozlowski LT, Frecker RC, Fagerstrom K-O. The Fagerstrom test for nicotine dependence: a revision of the Fagerstrom tolerance questionnaire. Br J Addict. 1991;86(9):1119–27.Google Scholar
  27. 27.
    Russell DW. UCLA loneliness scale (version 3): reliability, validity, and factor structure. J Pers Assess. 1996;66(1):20–40.Google Scholar
  28. 28.
    Ware JE, Sherbourne CD. The MOS 36-Item-Short-Form Health Survey (SF-36): I. Conceptual framework and item selection. Med Care. 1992;30(6):473–83.Google Scholar
  29. 29.
    Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1(3):385–401.Google Scholar
  30. 30.
    Basco MR, Krebaum SR, Rush AJ. Outcome measures of depression. In: Strupp HH, Horowitz LM, Lambert MJ, editors. Measuring patient changes in mood, anxiety, and personality disorders. Washington, DC: American Psychological Association; 1997. p. 207–45.Google Scholar
  31. 31.
    Dohrenwend BP. Inventorying stressful life events as risk factors dor psychopathology: toward resolution of the problem of intracategory variability. Psychol Bull. 2006;132(3):477–95.Google Scholar
  32. 32.
    Dohrenwend BS, Krasnoff L, Askenasy AR, Dohrenwend BP. Exemplification of a method for scaling life events: the PERI life events scale. J Health Soc Behav. 1978;19(2):205–29.Google Scholar
  33. 33.
    Bernstein DP, Fink L, Handelsman L, Foote J, Lovejoy M, Wenzel K, Sapareto E, Ruggiero J. Initial reliability and validity of a new retrospective measure of child abuse and neglect. Am J Psychiatr. 1994;151(8):1132–6.Google Scholar
  34. 34.
    Bernstein DP, Fink L. Childhood trauma questionnaire: a retrospective self-report. San Antonio, TX: The Psychological Corporation; 1998.Google Scholar
  35. 35.
    Buysse DJ, Reynolds CF, 3rd, Monk TH, Hoch CC, Yeager AL, Kupfer DJ. Quantification of subjective sleep quality in healthy elderly men and women using the Pittsburgh Sleep Quality Index (PSQI). Sleep. 1991;14(4):331–8.Google Scholar
  36. 36.
    Burnsides C, Corry J, Alexander J, Balint C, Cosmar D, Phillips G, Marketon JI. Ex vivo stimulation of whole blood as a means to determine glucocorticoid sensitivity. J Inflamm Res. 2012;5:89–97.Google Scholar
  37. 37.
    Jarczok MN, Kleber ME, Koenig J, Loerbroks A, Herr RM, Hoffmann K, Fischer JE, Benyamini Y, Thayer JF. Investigating the associations of self-rated health: heart rate variability is more strongly associated than inflammatory and other frequently used biomarkers in a cross sectional occupational sample. PLoS One. 2015;10(2):e0117196.Google Scholar
  38. 38.
    Jylhä M. What is self-rated health and why does it predict mortality? Towards a unified conceptual model. Soc Sci Med. 2009;69(3):307–16.Google Scholar
  39. 39.
    Rollema H, Russ C, Lee TC, Hurst RS, Bertrand D. Functional interactions of varenicline and nicotine with nAChR subtypes implicated in cardiovascular control. Nicotine Tob Res. 2014;16(6):733–42.Google Scholar
  40. 40.
    Harte CB, Meston CM. Effects of smoking cessation on heart rate variability among long-term male smokers. Int J Behav Med. 2014;21(2):302–9.Google Scholar
  41. 41.
    Dinas PC, Koutedakis Y, Flouris AD. Effects of active and passive tobacco cigarette smoking on heart rate variability. Int J Cardiol. 2013;163(2):109–15.Google Scholar
  42. 42.
    Childs E, de Wit H. Hormonal, cardiovascular, and subjective responses to acute stress in smokers. Psychopharmacology. 2009;203(1):1–12.Google Scholar
  43. 43.
    al’Absi M, Wittmers LE, 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(2):401–10.Google Scholar
  44. 44.
    Kirschbaum C, Strasburger CJ, Langkrar J. Attenuated cortisol response to psychological stress but not to CRH or ergometry in young habitual smokers. Pharmacol Biochem Behav. 1993;44(3):527–31.Google Scholar
  45. 45.
    Kirschbaum C, Scherer G, Strasburger CJ. Pituitary and adrenal hormone responses to pharmacological, physical, and psychological stimulation in habitual smokers and nonsmokers. Clin Investig. 1994;72(10):804–10.Google Scholar
  46. 46.
    Childs E, de Wit H. Effects of acute psychosocial stress on cigarette craving and smoking. Nicotine Tob Res. 2010;12(4):449–53.Google Scholar
  47. 47.
    Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ. Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation. Nature. 2003;421(6921):384–8.Google Scholar
  48. 48.
    Tracey KJ. Physiology and immunology of the cholinergic antiinflammatory pathway. J Clin Investig. 2007;117(2):289–96.Google Scholar
  49. 49.
    Dao DQ, Salas R, De Biasi M. Nicotinic acetylcholine receptors along the Habenulo-interpeduncular pathway: roles in nicotine withdrawal and other aversive aspects. In: Lester R, editor. Nicotinic receptors. New York, NY; Humana Press; 2014. p. 363–82.Google Scholar
  50. 50.
    Leary MR, Cox CB. Belongingness motivation: a mainspring of social action. Handbook of motivation science. New York: Guilford Press; 2008. p. 27–40.Google Scholar
  51. 51.
    Tooby J, Cosmides L. Friendship and the banker’s paradox: other pathways to the evolution of adaptations for altruism. Paper presented at: Proceedings British Academy; 1996.Google Scholar
  52. 52.
    Baumeister RF, Leary MR. The need to belong: desire for interpersonal attachments as a fundamental human motivation. Psychol Bull. 1995;117(3):497.Google Scholar
  53. 53.
    Holt-Lunstad J, Smith TB, Layton JB. Social relationships and mortality risk: a meta-analytic review. PLoS Med. 2010;7(7):e1000316.Google Scholar
  54. 54.
    Holwerda TJ, van Tilburg TG, Deeg DJH, Schutter N, Van R, Dekker J, Stek ML, Beekman AT, Schoevers RA. Impact of loneliness and depression on mortality: results from the Longitudinal Ageing Study Amsterdam. Br J Psychiatry. 2016;209(2):127–34.Google Scholar
  55. 55.
    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(7455):1519.Google Scholar
  56. 56.
    Sugisawa H, Liang J, Liu X. Social networks, social support, and mortality among older people in Japan. J Gerontol. 1994;49(1):S3–13.Google Scholar
  57. 57.
    Thurston RC, Kubzansky LD. Women, loneliness, and incident coronary heart disease. Psychosom Med. 2009;71(8):836–42.Google Scholar
  58. 58.
    Dixon D, Cruess S, Kilbourn K, Klimas N, Fletcher M, Ironson G, Baum A, Schneiderman N, Antoni MH. Social support mediates loneliness and human herpesvirus type 6 (HHV 6) antibody titers. J Appl Soc Psychol. 2001;31(6):1111–32.Google Scholar
  59. 59.
    Hawkley LC, Masi CM, Berry JD, Cacioppo JT. Loneliness is a unique predictor of age-related differences in systolic blood pressure. Psychol Aging. 2006;21(1):152.Google Scholar
  60. 60.
    Hawkley LC, Thisted RA, Masi CM, Cacioppo JT. Loneliness predicts increased blood pressure: 5-year cross-lagged analyses in middle-aged and older adults. Psychol Aging. 2010;25(1):132.Google Scholar
  61. 61.
    Shields GS, Moons WG, Slavich GM. Inflammation, self-regulation, and health: an immunologic model of self-regulatory failure. Perspect Psychol Sci. 2017;12(4):588–612.Google Scholar
  62. 62.
    Sturmberg JP, Bennett JM, Martin CM, Picard M. ‘Multimorbidity’ as the manifestation of network disturbances. J Eval Clin Pract. 2017;23(1):199–208.Google Scholar
  63. 63.
    Ford DH. Humans as self-constructing living systems. 2nd ed. State College, PA: Ideals; 1994.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Jeanette M. Bennett
    • 1
  • Lydia G. Roos
    • 2
  • Joseph S. Marino
    • 3
  • Nicolas Rohleder
    • 4
    • 5
  • Maren J. Coffman
    • 6
  1. 1.Department of Psychological Science and Health Psychology PhD ProgramThe University of North Carolina at CharlotteCharlotteUSA
  2. 2.Health Psychology PhD ProgramThe University of North Carolina at CharlotteCharlotteUSA
  3. 3.Department of KinesiologyThe University of North Carolina at CharlotteCharlotteUSA
  4. 4.Department of Psychology and Sports ScienceFriedrich-Alexander-University of Erlangen-Nürnberg ErlangenErlangenGermany
  5. 5.Department of PsychologyBrandeis UniversityWalthamUSA
  6. 6.School of Nursing and Health Psychology PhD ProgramThe University of North Carolina at CharlotteCharlotteUSA

Personalised recommendations