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Positive and Negative Affect and Salivary Markers of Inflammation Among Young Adults

  • Special Issue: Salivary Bioscience
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Abstract

Background

Emerging evidence suggests that higher circulating levels of inflammatory biomarkers in blood are associated with higher negative affect (NA) and lower positive affect (PA). To our knowledge, the unique associations between NA and PA in daily life and salivary biomarkers of inflammation have not been examined. This study examined these associations in young adults.

Methods

Measures of NA and PA were created from aggregated daily measures of affect (morning and evening ratings averaged across 14 days). We investigated associations between these measures and salivary C-reactive protein (CRP) and interleukin (IL)-6 in a sample of 108 young adults (60% female, mean age = 20.45 ± 1.47), a subset of whom had self-reported chronic back pain (n = 49). CRP and IL-6 were determined from saliva obtained at the end of the daily diary period.

Results

After covarying for age, gender, body mass index, chronic pain status, salivary flow rate, and NA, higher PA was associated with lower salivary CRP (β = − 0.02, 95% CI (− 0.03, − 0.00) sr2 = .06, p = .01) but not IL-6; removing NA from this model did not change results. In a model with the same covariates (and PA), NA was not significantly related to CRP or IL-6. Chronic back pain status and gender did not moderate results.

Conclusions

Findings suggest that higher PA may be associated with lower salivary CRP in young adults, even after accounting for NA and demographic characteristics. Findings highlight the utility of assessing emotional states in relation to salivary markers of inflammation in future biobehavioral research.

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References

  1. Andreasson AN, Szulkin R, Undén A-L, von Essen J, Nilsson L-G, Lekander M. Inflammation and positive affect are associated with subjective health in women of the general population. J Health Psychol. 2013;18(3):311–20.

    Article  PubMed  Google Scholar 

  2. Brouwers C, Mommersteeg PMC, Nyklíček I, Pelle AJ, Westerhuis BLWJJM, Szabó BM, et al. Positive affect dimensions and their association with inflammatory biomarkers in patients with chronic heart failure. Biol Psychol. 2013;92(2):220–6.

  3. Chauhan A, Yadav SS, Dwivedi P, Lal N, Usman K, Khattri S. Correlation of serum and salivary cytokines level with clinical parameters in metabolic syndrome with periodontitis. J Clin Lab Anal. 2016;30(5):649–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chida Y, Steptoe A. Positive psychological well-being and mortality: a quantitative review of prospective observational studies. Psychosom Med. 2008;70(7):741–56.

    Article  PubMed  Google Scholar 

  5. Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. Hillsdale: Lawrence Earlbaum Associates; 1988.

    Google Scholar 

  6. Consedine NS, Moskowitz JT. The role of discrete emotions in health outcomes: a critical review. Appl Prev Psychol. 2007;12(2):59–75.

    Article  Google Scholar 

  7. Cooper TM, McKinley PS, Seeman TE, Choo T-H, Lee S, Sloan RP. Heart rate variability predicts levels of inflammatory markers: evidence for the vagal anti-inflammatory pathway. Brain Behav Immun. 2015;49:94–100.

    Article  CAS  PubMed  Google Scholar 

  8. Cullen T, Thomas AW, Webb R, Hughes MG. The relationship between interleukin-6 in saliva, venous and capillary plasma, at rest and in response to exercise. Cytokine. 2015;71(2):397–400.

    Article  CAS  PubMed  Google Scholar 

  9. Dan H, Liu W, Wang J, Wang Z, Wu R, Chen Q, et al. Elevated IL-10 concentrations in serum and saliva from patients with oral lichen planus. Quintessence Int. 2011;42(2):157–63.

    PubMed  Google Scholar 

  10. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9(1):46–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Darnall BD, Suarez EC. Sex and gender in psychoneuroimmunology research: past, present and future. Brain Behav Immun. 2009;23(5):595–604.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Desai GS, Mathews ST. Saliva as a non-invasive diagnostic tool for inflammation and insulin-resistance. World J Diabetes. 2014;5(6):730–8.

    Article  PubMed  PubMed Central  Google Scholar 

  13. DeVon HA, Piano MR, Rosenfeld AG, Hoppensteadt DA. The association of pain with protein inflammatory biomarkers: a review of the literature. Nurs Res. 2014;63(1):51–62.

    Article  PubMed  Google Scholar 

  14. Ebersole JL, Kryscio RJ, Campbell C, Kinane DF, McDevitt J, Christodoulides N, et al. Salivary and serum adiponectin and C-reactive protein levels in acute myocardial infarction related to body mass index and oral health. J Periodontal Res. 2017;52(3):419–27.

    Article  CAS  PubMed  Google Scholar 

  15. Engeland C, Bosch J, Rohleder N. Salivary biomarkers in psychoneuroimmunology. Curr Opin Behav Sci. 2019;28:58–65.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Faul F, Erdfelder E, Lang A-G, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.

    Article  PubMed  Google Scholar 

  17. Fernandez-Botran R, Miller JJ, Burns VE, Newton TL. Correlations among inflammatory markers in plasma, saliva and oral mucosal transudate in post-menopausal women with past intimate partner violence. Brain Behav Immun. 2011;25:314–21.

    Article  CAS  PubMed  Google Scholar 

  18. Fillingim RB, King CD, Ribeiro-Dasilva MC, Rahim-Williams B, Riley JL. Sex, gender, and pain: a review of recent clinical and experimental findings. J Pain. 2009;10(5):447–85.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ford DE, Erlinger TP. Depression and C-reactive protein in US adults: Data from the Third National Health and nutrition examination survey. Arch Intern Med. 2004;164(9):1010–4.

    Article  PubMed  Google Scholar 

  20. Fredrickson BL. The broaden-and-build theory of positive emotions. Philos Trans R Soc B Biol Sci. 2004;359(1449):1367–78.

    Article  Google Scholar 

  21. Fredrickson BL, Levenson RW. Positive emotions speed recovery from the cardiovascular sequelae of negative emotions. Cognit Emot. 1998;12:191–220.

    Article  Google Scholar 

  22. Friedman EM, Hayney M, Love GD, Singer BH, Ryff CD. Plasma interleukin-6 and soluble IL-6 receptors are associated with psychological well-being in aging women. Health Psychol. 2007;26(3):305–13.

    Article  PubMed  Google Scholar 

  23. Gohel V, Jones JA, Wehler CJ. Salivary biomarkers and cardiovascular disease: a systematic review. Clin Chem Lab Med. 2018;56(9):1432–42.

    Article  CAS  PubMed  Google Scholar 

  24. Graham JE, Robles TF, Kiecolt-Glaser JK, Malarkey WB, Bissell MG, Glaser R. Hostility and pain are related to inflammation in older adults. Brain Behav Immun. 2006;20:389–400.

    Article  CAS  PubMed  Google Scholar 

  25. Graham-Engeland JE, Sin NL, Smyth JM, Jones DR, Knight EL, Sliwinski MJ, et al. Negative and positive affect as predictors of inflammation: timing matters. Brain Behav Immun. 2018;74:222–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Granger DA, Kivlighan KT, Fortunato C, Harmon AG, Hibel LC, Schwartz EB, et al. Integration of salivary biomarkers into developmental and behaviorally-oriented research: problems and solutions for collecting specimens. Physiol Behav. 2007;92(4):583–90.

  27. Granger DA, Johnson SB, Szanton SL, Out D, Schumann LL. Incorporating salivary biomarkers into nursing research: an overview and review of best practices. Biol Res Nurs. 2012;14(4):347–56.

    Article  PubMed  Google Scholar 

  28. Hoyt MA, Stanton AL, Bower JE, Thomas KS, Litwin MS, Breen EC, et al. Inflammatory biomarkers and emotional approach coping in men with prostate cancer. Brain Behav Immun. 2013;32:173–9.

  29. Ironson G, Banerjee N, Fitch C, Krause N. Positive emotional well-being, health behaviors, and inflammation measured by C-reactive protein. Soc Sci Med. 2018;197:235–43.

    Article  PubMed  Google Scholar 

  30. Irwin MR, Olmstead R, Carroll JE. Sleep disturbance, sleep duration, and inflammation: a systematic review and meta-analysis of cohort studies and experimental sleep deprivation. Biol Psychiatry. 2016;80(1):40–52.

    Article  PubMed  Google Scholar 

  31. Iyengar A, Paulus JK, Gerlanc DJ, Maron JL. Detection and potential utility of C-reactive protein in saliva of neonates. Front Pediatr. 2014;2:131.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Izawa S, Miki K, Liu X, Ogawa N. The diurnal patterns of salivary interleukin-6 and C-reactive protein in healthy young adults. Brain Behav Immun. 2013;27:38–41.

    Article  CAS  PubMed  Google Scholar 

  33. Janicki-Deverts D, Cohen S, Doyle WJ, Turner RB, Treanor JJ. Infection-induced proinflammatory cytokines are associated with decreases in positive affect, but not increases in negative affect. Brain Behav Immun. 2007;21(3):301–7.

    Article  CAS  PubMed  Google Scholar 

  34. Kiecolt-Glaser JK, McGuire L, Robles TR, Glaser R. Emotions, morbidity, and mortality: new perspectives from psychoneuroimmunology. Annu Rev Psychol. 2002;53:83–107.

    Article  PubMed  Google Scholar 

  35. Kopanczyk R, Opris DC, Lickliter J, Bridges EG, Nazar AM, Bridges KG. C-reactive protein levels in blood and saliva show no correlation in young, healthy adults. FASEB J. 2010;24:lb409.

    Article  Google Scholar 

  36. Kubzansky LD, Kawachi I. Going to the heart of the matter: do negative emotions cause coronary heart disease? J Psychosom Res. 2000;48(4–5):323–37.

    Article  CAS  PubMed  Google Scholar 

  37. La Fratta I, Tatangelo R, Campagna G, Rizzuto A, Franceschelli S, Ferrone A, et al. The plasmatic and salivary levels of IL-1β, IL-18 and IL-6 are associated to emotional difference during stress in young male. Sci Rep. 2018;8(1):3031.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Lin C, Michopoulos V, Powers A, Wingo AP, Schwartz A, Bradley B, et al. Affect, inflammation, and health in urban at-risk civilians. J Psychiatr Res. 2018;104:24–31.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Majd M, Graham-Engeland JE, Smyth JM, Sliwinski MJ, Lipton RB, Katz MJ, et al. Distinct inflammatory response patterns are evident among men and women with higher depressive symptoms. Physiol Behav. 2018;184:108–15.

  40. Marsland AL, Pressman S, Cohen S. Positive affect and immune function. Psychoneuroimmunology. 2007:261–79.

  41. Meier-Ewert HK, Ridker PM, Rifai N, Price N, Dinges DF, Mullington JM. Absence of diurnal variation of C-reactive protein concentrations in healthy human subjects. Clin Chem. 2001;47(3):426–30.

    Article  CAS  PubMed  Google Scholar 

  42. Miyamoto Y, Boylan JM, Coe CL, Curhan KB, Levine CS, Markus HR, et al. Negative emotions predict elevated interleukin-6 in the United States but not in Japan. Brain Behav Immun. 2013;34:79–85.

    Article  CAS  PubMed  Google Scholar 

  43. Mortensen RF. C-reactive protein, inflammation, and innate immunity. Immunol Res. 2001;24(2):163–76.

    Article  CAS  PubMed  Google Scholar 

  44. Newton TL, Fernandez-Botran R, Miller JJ, Burns VE. Interleukin-6 and soluble interleukin-6 receptor levels in posttraumatic stress disorder: associations with lifetime diagnostic status and psychological context. Biol Psychol. 2014;99:150–9.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Newton TL, Fernandez-Botran R, Lyle KB, Szabo YZ, Miller JJ, Warnecke AJ. Salivary cytokine response in the aftermath of stress: an emotion regulation perspective. Emotion. 2017;17(6):1007–20.

    Article  PubMed  Google Scholar 

  46. Nishanian P, Aziz N, Chung J, Detels R, Fahey JL. Oral fluids as an alternative to serum for measurement of markers of immune activation. Clin Diagn Lab Immunol. 1998;5(4):507–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. O’Connor MF, Bower JE, Cho HJ, Creswell JD, Dimitrov S, Hamby ME, et al. To assess, to control, to exclude: effects of biobehavioral factors on circulating inflammatory markers. Brain Behav Immun. 2009;23(7):887–97.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Ong AD, Benson L, Zautra AJ, Ram N. Emodiversity and biomarkers of inflammation. Emotion. 2018;18(1):3–14.

    Article  PubMed  Google Scholar 

  49. Ouellet-Morin I, Danese A, Williams B, Arseneault L. Validation of a high-sensitivity assay for C-reactive protein in human saliva. Brain Behav Immun. 2011;25:640–6.

    Article  CAS  PubMed  Google Scholar 

  50. Out D, Hall RJ, Granger DA, Page GG, Woods SJ. Assessing salivary C-reactive protein: longitudinal associations with systemic inflammation and cardiovascular disease risk in women exposed to intimate partner violence. Brain Behav Immun. 2012;26(4):543–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Prather AA, Marsland AL, Muldoon MF, Manuck SB. Positive affective style covaries with stimulated IL-6 and IL-10 production in a middle-aged community sample. Brain Behav Immun. 2007;21(8):1033–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Pressman SD, Cohen S. Does positive affect influence health? Psychological Bulletin. 2005;131(6):925–971.

  53. R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2013. Retrieved from http://www.R-project.org/. Accessed 1 March 2019

  54. Silvestre-Rangil J, Bagán L, Silvestre FJ, Martinez-Herrera M, Bagán J. Periodontal, salivary and IL-6 status in rheumatoid arthritis patients. A cross-sectional study. Med Oral Patol Oral Cir Bucal. 2017;22(5):e595–600. Retrieved from. https://doi.org/10.4317/medoral.21937.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Sin NL, Graham-Engeland JE, Almeida DM. Daily positive events and inflammation: findings from the National Study of Daily Experiences. Brain Behav Immun. 2015a;43:130–8.

    Article  PubMed  Google Scholar 

  56. Sin NL, Graham-Engeland JE, Ong AD, Almeida DM. Affective reactivity to daily stressors is associated with elevated inflammation. Health Psychol. 2015b;34(12):1154–65.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Slavish DC, Graham-Engeland JE, Smyth JM, Engeland CG. Salivary markers of inflammation in response to acute stress. Brain Behav Immun. 2014;44:253–69.

    Article  PubMed  CAS  Google Scholar 

  58. Smyth JM, Stone AA. Ecological momentary assessment research in behavioral medicine. J Happiness Stud. 2003;4(1):35–52.

    Article  Google Scholar 

  59. Stanley D. apaTables: create American Psychological Association (APA) Style Tables (Version 1.5.1) [R package]; 2017. Retrieved from https://github.com/dstanley4/apaTables. Accessed 1 March 2019

  60. Stellar JE, John-Henderson N, Anderson CL, Gordon AM, McNeil GD, Keltner D. Positive affect and markers of inflammation: discrete positive emotions predict lower levels of inflammatory cytokines. Emotion. 2015;15(2):129–33.

    Article  PubMed  Google Scholar 

  61. Steptoe A, Leigh Gibson E, Hamer M, Wardle J. Neuroendocrine and cardiovascular correlates of positive affect measured by ecological momentary assessment and by questionnaire. Psychoneuroendocrinology. 2007;32(1):56–64.

    Article  CAS  PubMed  Google Scholar 

  62. Sterne JAC, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, et al. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ. 2009;338:b2393.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Sturgeon JA, Arewasikporn A, Okun MA, Davis MC, Ong AD, Zautra AJ. The psychosocial context of financial stress: implications for inflammation and psychological health. Psychosom Med. 2016;78(2):134–43.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Szabo YZ, Fernandez-Botran R, Newton TL. Cumulative trauma, emotion reactivity and salivary cytokine levels following acute stress in healthy women. Anxiety Stress Coping. 2018;20:1–13.

    Google Scholar 

  65. Uchino BN, Trettevik R, Kent de Grey RG, Cronan S, Hogan J, Baucom BRW. Social support, social integration, and inflammatory cytokines: a meta-analysis. Health Psychol. 2018;37(5):462–71.

    Article  PubMed  Google Scholar 

  66. Vgontzas AN, Bixler EO, Lin HM, Prolo P, Trakada G, Chrousos GP. IL-6 and its circadian secretion in humans. Neuroimmunomodulation. 2005;12(3):131–40.

    Article  CAS  PubMed  Google Scholar 

  67. Watkins LR, Maier SF, Goehler LE. Immune activation: the role of pro-inflammatory cytokines in inflammation, illness responses and pathological pain states. Pain. 1995;63:289–302.

    Article  PubMed  Google Scholar 

  68. Watson D, Clark LA, Tellegen A. Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol. 1988;54:1063–70.

    Article  CAS  PubMed  Google Scholar 

  69. Weiser EB. Associations between positive and negative affect and 12-month physical disorders in a national sample. J Clin Psychol Med Settings. 2012;19(2):197–210.

    Article  PubMed  Google Scholar 

  70. Williamson S, Munro C, Pickler R, Grap MJ, Elswick R. Comparison of biomarkers in blood and saliva in healthy adults. Nurs Res Pract. 2012;2012.

  71. Woods JA, Vieira VJ, Keylock KT. Exercise, inflammation, and innate immunity. Neurol Clin. 2009;29(2):381–93.

    Google Scholar 

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Acknowledgments

The authors would like to thank Matthew Ulrich for his assistance running the inflammatory assays.

Funding

This study was funded in part by the Social Science Research Institute at the Penn State University (PI: Graham-Engeland). Jones was supported by National Institutes of Aging T32AG049676 to the Pennsylvania State University. Song was supported by the National Research Foundation of Korea’s Brain Korea 21 PLUS (Embodiment: Health and Society Interaction) to Korea University.

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Authors and Affiliations

  1. Department of Psychology, University of North Texas, Denton, TX, USA

    Danica C. Slavish

  2. Department of Biobehavioral Health, The Pennsylvania State University, University Park, PA, USA

    Dusti R. Jones, Joshua M. Smyth, Christopher G. Engeland, Nolan M. McCormick & Jennifer E. Graham-Engeland

  3. Center for Healthy Aging, The Pennsylvania State University, University Park, PA, USA

    Dusti R. Jones, Joshua M. Smyth & Christopher G. Engeland

  4. Department of Medicine, The Pennsylvania State University, Hershey, PA, USA

    Joshua M. Smyth

  5. College of Nursing, The Pennsylvania State University, University Park, PA, USA

    Christopher G. Engeland

  6. Department of Public Health Sciences, BK21PLUS Program in Embodiment: Health-Society Interaction, Graduate School, Korea University, Seoul, South Korea

    Sunmi Song

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  1. Danica C. Slavish
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Correspondence to Danica C. Slavish.

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Slavish, D.C., Jones, D.R., Smyth, J.M. et al. Positive and Negative Affect and Salivary Markers of Inflammation Among Young Adults. Int.J. Behav. Med. 27, 282–293 (2020). https://doi.org/10.1007/s12529-019-09795-2

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