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Mood disorders and circulating levels of inflammatory markers in a longitudinal population-based study

Published online by Cambridge University Press:  20 September 2017

J. Glaus ,
R. von Känel ,
A. M. Lasserre ,
M.-P. F. Strippoli ,
C. L. Vandeleur ,
E. Castelao ,
M. Gholam-Rezaee ,
C. Marangoni ,
E.-Y. N. Wagner  and
P. Marques-Vidal
...Show all authors
J. Glaus*
Affiliation:
Department of Psychiatry, Psychiatric Epidemiology and Psychopathology Research Center, Lausanne University Hospital, Lausanne, Switzerland Genetic Epidemiology Research Branch, Intramural Research Program, National Institute of Mental Health, Bethesda, MD, USA
R. von Känel
Affiliation:
Department of Psychosomatic Medicine, Clinic Barmelweid, Barmelweid, Switzerland Department of Neurology, Inselspital, Bern University Hospital, and University of Bern, Bern, Switzerland
A. M. Lasserre
Affiliation:
Department of Psychiatry, Psychiatric Epidemiology and Psychopathology Research Center, Lausanne University Hospital, Lausanne, Switzerland
M.-P. F. Strippoli
Affiliation:
Department of Psychiatry, Psychiatric Epidemiology and Psychopathology Research Center, Lausanne University Hospital, Lausanne, Switzerland
C. L. Vandeleur
Affiliation:
Department of Psychiatry, Psychiatric Epidemiology and Psychopathology Research Center, Lausanne University Hospital, Lausanne, Switzerland
E. Castelao
Affiliation:
Department of Psychiatry, Psychiatric Epidemiology and Psychopathology Research Center, Lausanne University Hospital, Lausanne, Switzerland
M. Gholam-Rezaee
Affiliation:
Department of Psychiatry, Psychiatric Epidemiology and Psychopathology Research Center, Lausanne University Hospital, Lausanne, Switzerland
C. Marangoni
Affiliation:
Genetic Epidemiology Research Branch, Intramural Research Program, National Institute of Mental Health, Bethesda, MD, USA
E.-Y. N. Wagner
Affiliation:
Department of Neurology, Inselspital, Bern University Hospital, and University of Bern, Bern, Switzerland
P. Marques-Vidal
Affiliation:
Department of Internal Medicine, Lausanne University Hospital, Lausanne, Switzerland
G. Waeber
Affiliation:
Department of Internal Medicine, Lausanne University Hospital, Lausanne, Switzerland
P. Vollenweider
Affiliation:
Department of Internal Medicine, Lausanne University Hospital, Lausanne, Switzerland
M. Preisig
Affiliation:
Department of Psychiatry, Psychiatric Epidemiology and Psychopathology Research Center, Lausanne University Hospital, Lausanne, Switzerland
K. R. Merikangas
Affiliation:
Genetic Epidemiology Research Branch, Intramural Research Program, National Institute of Mental Health, Bethesda, MD, USA
*
*Address for correspondence: J. Glaus, Genetic Epidemiology Research Branch, Intramural Research Program, National Institute of Mental Health, 35 Convent Drive, MSC 3720, Bldg 35A, Room 2E422A, Bethesda, MD 20892, USA. (Email: jennifer.glaus@nih.gov)
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Abstract

Background

There has been increasing evidence that chronic low-grade inflammation is associated with mood disorders. However, the findings have been inconsistent because of heterogeneity across studies and methodological limitations. Our aim is to prospectively evaluate the bi-directional associations between inflammatory markers including interleukin (IL)-6, tumor necrosis factor (TNF)-α and high sensitivity C-reactive protein (hsCRP) with mood disorders.

Methods

The sample consisted of 3118 participants (53.7% women; mean age: 51.0, s.d. 8.8 years), randomly selected from the general population, who underwent comprehensive somatic and psychiatric evaluations at baseline and follow-up (mean follow-up duration = 5.5 years, s.d. 0.6). Current and remitted mood disorders including bipolar and major depressive disorders (MDD) and its subtypes (atypical, melancholic, combined atypical and melancholic, and unspecified) were based on semi-structured diagnostic interviews. Inflammatory biomarkers were analyzed in fasting blood samples. Associations were tested by multiple linear and logistic regression models.

Results

Current combined MDD [β = 0.29, 95% confidence interval (CI) 0.03–0.55] and current atypical MDD (β = 0.32, 95% CI 0.10–0.55) at baseline were associated with increased levels of hsCRP at follow-up. There was little evidence for inflammation markers at baseline predicting mood disorders at follow-up.

Conclusions

The prospective unidirectional association between current MDD subtype with atypical features and hsCRP levels at follow-up suggests that inflammation may be a consequence of this condition. The role of inflammation, particularly hsCRP that is critically involved in cardiovascular diseases, warrants further study. Future research that examines potential influences of medications on inflammatory processes is indicated.

Keywords

Atypical depressioncardiovascular risk factorsC-reactive proteinmood disorderspro-inflammatory cytokinesprospective study
Type
Original Articles
Information
Psychological Medicine , Volume 48 , Issue 6 , April 2018 , pp. 961 - 973
Copyright
Copyright © Cambridge University Press 2017 

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References

Achur, RN, Freeman, WM, Vrana, KE (2010). Circulating cytokines as biomarkers of alcohol abuse and alcoholism. Journal of Neuroimmune Pharmacology 5, 83–91.CrossRefGoogle ScholarPubMed
Agosti, V, Levin, FR (2006). The effects of alcohol and drug dependence on the course of depression. The American Journal on Addictions 15, 71–75.Google Scholar
Angst, J, Gamma, A, Benazzi, F, Silverstein, B, Ajdacic-Gross, V, Eich, D, Rossler, W (2006). Atypical depressive syndromes in varying definitions. European Archives of Psychiatry and Clinical Neuroscience 256, 44–54.Google Scholar
Anthenelli, RM (2010). Focus on: comorbid mental health disorders. Alcohol Research & Health 33, 109–117.Google Scholar
Baune, BT, Stuart, M, Gilmour, A, Wersching, H, Arolt, V, Berger, K (2012). Moderators of the relationship between depression and cardiovascular disorders: a systematic review. General Hospital Psychiatry 34, 478–492.Google Scholar
Benjamini, Y, Hochberg, Y (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289–300.Google Scholar
Berney, A, Preisig, M, Matthey, ML, Ferrero, F, Fenton, BT (2002). Diagnostic interview for genetic studies (DIGS): inter-rater and test-retest reliability of alcohol and drug diagnoses. Drug and Alcohol Dependence 65, 149–158.Google Scholar
Chaiton, MO, Cohen, JE, O'Loughlin, J, Rehm, J (2009). A systematic review of longitudinal studies on the association between depression and smoking in adolescents. BMC Public Health 9, 356.Google Scholar
Charlson, FJ, Moran, AE, Freedman, G, Norman, RE, Stapelberg, NJ, Baxter, AJ, Vos, T, Whiteford, HA (2013). The contribution of major depression to the global burden of ischemic heart disease: a comparative risk assessment. BMC Medicine 11, 250.Google Scholar
Chocano-Bedoya, PO, Mirzaei, F, O'Reilly, EJ, Lucas, M, Okereke, OI, Hu, FB, Rimm, EB, Ascherio, A (2014). C-reactive protein, interleukin-6, soluble tumor necrosis factor alpha receptor 2 and incident clinical depression. Journal of Affective Disorders 163, 25–32.Google Scholar
Copeland, WE, Shanahan, L, Worthman, C, Angold, A, Costello, EJ (2012). Cumulative depression episodes predict later C-reactive protein levels: a prospective analysis. Biological Psychiatry 71, 15–21.Google Scholar
Cunha, AB, Andreazza, AC, Gomes, FA, Frey, BN, da Silveira, LE, Goncalves, CA, Kapczinski, F (2008). Investigation of serum high-sensitive C-reactive protein levels across all mood states in bipolar disorder. European Archives of Psychiatry and Clinical Neuroscience 258, 300–304.Google Scholar
Dowlati, Y, Herrmann, N, Swardfager, W, Liu, H, Sham, L, Reim, EK, Lanctot, KL (2010). A meta-analysis of cytokines in major depression. Biological Psychiatry 67, 446–457.Google Scholar
Duivis, HE, de Jonge, P, Penninx, BW, Na, BY, Cohen, BE, Whooley, MA (2011). Depressive symptoms, health behaviors, and subsequent inflammation in patients with coronary heart disease: prospective findings from the heart and soul study. The American Journal of Psychiatry 168, 913–920.CrossRefGoogle ScholarPubMed
Endicott, J, Spitzer, RL (1978). A diagnostic interview: the schedule for affective disorders and schizophrenia. Archives of General Psychiatry 35, 837–844.CrossRefGoogle ScholarPubMed
Fernandes, BS, Steiner, J, Molendijk, ML, Dodd, S, Nardin, P, Goncalves, CA, Jacka, F, Kohler, CA, Karmakar, C, Carvalho, AF, Berk, M (2016). C-reactive protein concentrations across the mood spectrum in bipolar disorder: a systematic review and meta-analysis. Lancet Psychiatry 21, 554–564.Google Scholar
Firmann, M, Mayor, V, Vidal, PM, Bochud, M, Pecoud, A, Hayoz, D, Paccaud, F, Preisig, M, Song, KS, Yuan, X, Danoff, TM, Stirnadel, HA, Waterworth, D, Mooser, V, Waeber, G, Vollenweider, P (2008). The CoLaus study: a population-based study to investigate the epidemiology and genetic determinants of cardiovascular risk factors and metabolic syndrome. BMC Cardiovascular Disorders 8, 6.CrossRefGoogle ScholarPubMed
GBD 2015 DALYs & HALE Collaborators (2016). Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990–2015: a systematic analysis for the global burden of disease study 2015. Lancet 388, 1603–1658.CrossRefGoogle Scholar
Gimeno, D, Kivimaki, M, Brunner, EJ, Elovainio, M, De Vogli, R, Steptoe, A, Kumari, M, Lowe, GD, Rumley, A, Marmot, MG, Ferrie, JE (2009). Associations of C-reactive protein and interleukin-6 with cognitive symptoms of depression: 12-year follow-up of the Whitehall II study. Psychological Medicine 39, 413–423.Google Scholar
Glaus, J, Vandeleur, C, Gholam-Rezaee, M, Castelao, E, Perrin, M, Rothen, S, Bovet, P, Marques-Vidal, P, von Kanel, R, Merikangas, K, Mooser, V, Waterworth, DM, Waeber, G, Vollenweider, P, Preisig, M (2013). Atypical depression and alcohol misuse are related to the cardiovascular risk in the general population. Acta Psychiatrica Scandinavica 128, 282–293.Google Scholar
Glaus, J, Vandeleur, CL, von Kanel, R, Lasserre, AM, Strippoli, MP, Gholam-Rezaee, M, Castelao, E, Marques-Vidal, P, Bovet, P, Merikangas, K, Mooser, V, Waeber, G, Vollenweider, P, Aubry, JM, Preisig, M (2014). Associations between mood, anxiety or substance use disorders and inflammatory markers after adjustment for multiple covariates in a population-based study. Journal of Psychiatric Research 58, 36–45.Google Scholar
Hamer, M (2007). The relative influences of fitness and fatness on inflammatory factors. Preventive Medicine 44, 3–11.Google Scholar
Hickman, RJ, Khambaty, T, Stewart, JC (2014). C-reactive protein is elevated in atypical but not nonatypical depression: data from the National Health and Nutrition Examination survey (NHANES) 1999–2004. Journal of Behavioral Medicine 37, 621–629.Google Scholar
Hollingshead, AB (1975). Four Factor Index of Social Status. Unpublished manuscript, Yale University Press, New Haven, CT.Google Scholar
Howren, MB, Lamkin, DM, Suls, J (2009). Associations of depression with C-reactive protein, IL-1, and IL-6: a meta-analysis. Psychosomatic Medicine 71, 171–186.Google Scholar
Kaestner, F, Hettich, M, Peters, M, Sibrowski, W, Hetzel, G, Ponath, G, Arolt, V, Cassens, U, Rothermundt, M (2005). Different activation patterns of proinflammatory cytokines in melancholic and non-melancholic major depression are associated with HPA axis activity. Journal of Affective Disorders 87, 305–311.Google Scholar
Kiecolt-Glaser, JK, Derry, HM, Fagundes, CP (2015). Inflammation: depression fans the flames and feasts on the heat. The American Journal of Psychiatry 172, 1075–1091.Google Scholar
Kivimaki, M, Shipley, MJ, Batty, GD, Hamer, M, Akbaraly, TN, Kumari, M, Jokela, M, Virtanen, M, Lowe, GD, Ebmeier, KP, Brunner, EJ, Singh-Manoux, A (2014). Long-term inflammation increases risk of common mental disorder: a cohort study. Molecular Psychiatry 19, 149–150.Google Scholar
Lamers, F, Vogelzangs, N, Merikangas, KR, de Jonge, P, Beekman, AT, Penninx, BW (2013). Evidence for a differential role of HPA-axis function, inflammation and metabolic syndrome in melancholic versus atypical depression. Molecular Psychiatry 18, 692–699.Google Scholar
Lasserre, AM, Glaus, J, Vandeleur, CL, Marques-Vidal, P, Vaucher, J, Bastardot, F, Waeber, G, Vollenweider, P, Preisig, M (2014). Depression with atypical features and increase in obesity, body mass index, waist circumference, and fat mass: a prospective, population-based study. JAMA Psychiatry 71, 880–888.CrossRefGoogle Scholar
Leboyer, M, Barbe, B, Gorwood, P, Teherani, M, Allilaire, JF, Preisig, M, Matthey, ML, Poyetton, V, Ferrero, F (1995). Interview Diagnostique pour les Etudes Génétiques. INSERM: Paris.Google Scholar
Leboyer, M, Maier, W, Teherani, M, Lichtermann, D, D'Amato, T, Franke, P, Lepine, JP, Minges, J, McGuffin, P (1991). The reliability of the SADS-LA in a family study setting. European Archives of Psychiatry and Clinical Neuroscience 241, 165–169.Google Scholar
Lopresti, AL, Maker, GL, Hood, SD, Drummond, PD (2014). A review of peripheral biomarkers in major depression: the potential of inflammatory and oxidative stress biomarkers. Progress in Neuro-Psychopharmacology & Biological Psychiatry 48, 102–111.Google Scholar
Luppino, FS, de Wit, LM, Bouvy, PF, Stijnen, T, Cuijpers, P, Penninx, BW, Zitman, FG (2010). Overweight, obesity, and depression: a systematic review and meta-analysis of longitudinal studies. Archives of General Psychiatry 67, 220–229.Google Scholar
Marques-Vidal, P, Bochud, M, Bastardot, F, Luscher, T, Ferrero, F, Gaspoz, JM, Paccaud, F, Urwyler, A, von Kanel, R, Hock, C, Waeber, G, Preisig, M, Vollenweider, P (2011). Levels and determinants of inflammatory biomarkers in a Swiss population-based sample (CoLaus study). PLoS ONE 6, e21002.Google Scholar
Marques-Vidal, P, Schmid, R, Bochud, M, Bastardot, F, von Kanel, R, Paccaud, F, Glaus, J, Preisig, M, Waeber, G, Vollenweider, P (2012a). Adipocytokines, hepatic and inflammatory biomarkers and incidence of type 2 diabetes. The CoLaus study. PLoS ONE 7, e51768.Google Scholar
Marques-Vidal, P, Velho, S, Waterworth, D, Waeber, G, von Kanel, R, Vollenweider, P (2012b). The association between inflammatory biomarkers and metabolically healthy obesity depends of the definition used. European Journal of Clinical Nutrition 66, 426–435.Google Scholar
Matthews, KA, Schott, LL, Bromberger, J, Cyranowski, J, Everson-Rose, SA, Sowers, MF (2007). Associations between depressive symptoms and inflammatory/hemostatic markers in women during the menopausal transition. Psychosomatic Medicine 69, 124–130.Google Scholar
Matthews, KA, Schott, LL, Bromberger, JT, Cyranowski, JM, Everson-Rose, SA, Sowers, M (2010). Are there bi-directional associations between depressive symptoms and C-reactive protein in mid-life women? Brain, Behavior, and Immunity 24, 96–101.Google Scholar
Mezuk, B, Eaton, WW, Albrecht, S, Golden, SH (2008). Depression and type 2 diabetes over the lifespan: a meta-analysis. Diabetes Care 31, 2383–2390.Google Scholar
Modabbernia, A, Taslimi, S, Brietzke, E, Ashrafi, M (2013). Cytokine alterations in bipolar disorder: a meta-analysis of 30 studies. Biological Psychiatry 74, 15–25.Google Scholar
Muneer, A (2016). Bipolar disorder: role of inflammation and the development of disease biomarkers. Psychiatry Investigation 13, 18–33.Google Scholar
Nurnberger, JI Jr., Blehar, MC, Kaufmann, CA, York-Cooler, C, Simpson, SG, Harkavy-Friedman, J, Severe, JB, Malaspina, D, Reich, T (1994). Diagnostic interview for genetic studies. Rationale, unique features, and training. NIMH genetics initiative. Archives of General Psychiatry 51, 849–859.Google Scholar
Pearson, TA, Mensah, GA, Alexander, RW, Anderson, JL, Cannon, ROI, Criqui, M, Fadl, YY, Fortmann, SP, Hong, Y, Myers, GL, Rifai, N, Smith, SC Jr., Taubert, K, Tracy, RP, Vinicor, F (2003). Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the centers for disease control and prevention and the American Heart Association. Circulation 107, 499–511.Google Scholar
Preisig, M, Fenton, BT, Matthey, ML, Berney, A, Ferrero, F (1999). Diagnostic interview for genetic studies (DIGS): inter-rater and test-retest reliability of the French version. European Archives of Psychiatry and Clinical Neuroscience 249, 174–179.Google Scholar
Preisig, M, Waeber, G, Vollenweider, P, Bovet, P, Rothen, S, Vandeleur, C, Guex, P, Middleton, L, Waterworth, D, Mooser, V, Tozzi, F, Muglia, P (2009). The PsyCoLaus study: methodology and characteristics of the sample of a population-based survey on psychiatric disorders and their association with genetic and cardiovascular risk factors. BMC Psychiatry 9, 9.Google Scholar
Rosenblat, JD, Cha, DS, Mansur, RB, McIntyre, RS (2014). Inflamed moods: a review of the interactions between inflammation and mood disorders. Progress in Neuro-Psychopharmacology & Biological Psychiatry 53, 23–34.Google Scholar
Rosmond, R, Bjorntorp, P (2000). The hypothalamic-pituitary-adrenal axis activity as a predictor of cardiovascular disease, type 2 diabetes and stroke. Journal of Internal Medicine 247, 188–197.Google Scholar
Rothermundt, M, Arolt, V, Fenker, J, Gutbrodt, H, Peters, M, Kirchner, H (2001). Different immune patterns in melancholic and non-melancholic major depression. European Archives of Psychiatry and Clinical Neuroscience 251, 90–97.Google Scholar
Rougemont-Buecking, A, Rothen, S, Jeanpretre, N, Lustenberger, Y, Vandeleur, CL, Ferrero, F, Preisig, M (2008). Inter-informant agreement on diagnoses and prevalence estimates of anxiety disorders: direct interview versus family history method. Psychiatry Research 157, 211–223.Google Scholar
Rudolf, S, Greggersen, W, Kahl, KG, Huppe, M, Schweiger, U (2014). Elevated IL-6 levels in patients with atypical depression but not in patients with typical depression. Psychiatry Research 217, 34–38.Google Scholar
Schmidt, FM, Lichtblau, N, Minkwitz, J, Chittka, T, Thormann, J, Kirkby, KC, Sander, C, Mergl, R, Fasshauer, M, Stumvoll, M, Holdt, LM, Teupser, D, Hegerl, U, Himmerich, H (2014). Cytokine levels in depressed and non-depressed subjects, and masking effects of obesity. Journal of Psychiatric Research 55, 29–34.Google Scholar
Schmidt, HD, Shelton, RC, Duman, RS (2011). Functional biomarkers of depression: diagnosis, treatment, and pathophysiology. Neuropsychopharmacology 36, 2375–2394.Google Scholar
Skeppholm, M, Wallen, NH, Blomback, M, Kallner, A (2008). Can both EDTA and citrate plasma samples be used in measurements of fibrinogen and C-reactive protein concentrations? Clinical Chemistry and Laboratory Medicine 46, 1175–1179.Google Scholar
Stewart, JC, Rand, KL, Muldoon, MF, Kamarck, TW (2009). A prospective evaluation of the directionality of the depression-inflammation relationship. Brain, Behavior, and Immunity 23, 936–944.Google Scholar
Tully, PJ, Baumeister, H, Bengel, J, Jenkins, A, Januszewski, A, Martin, S, Wittert, GA (2015). The longitudinal association between inflammation and incident depressive symptoms in men: the effects of hs-CRP are independent of abdominal obesity and metabolic disturbances. Physiology & Behavior 139, 328–335.Google Scholar
Valkanova, V, Ebmeier, KP, Allan, CL (2013). CRP, IL-6 and depression: a systematic review and meta-analysis of longitudinal studies. Journal of Affective Disorders 150, 736–744.Google Scholar
Van der Kooy, K, van Hout, H, Marwijk, H, Marten, H, Stehouwer, C, Beekman, A (2007). Depression and the risk for cardiovascular diseases: systematic review and meta analysis. International Journal of Geriatric Psychiatry 22, 613–626.Google Scholar
Wagner, EY, Wagner, JT, Glaus, J, Vandeleur, CL, Castelao, E, Strippoli, MP, Vollenweider, P, Preisig, M, von Kanel, R (2015). Evidence for chronic low-grade systemic inflammation in individuals with agoraphobia from a population-based prospective study. PLoS ONE 10, e0123757.Google Scholar
Watson, S, Mackin, P (2006). HPA axis function in mood disorders. Psychiatry 5, 166–170.Google Scholar
Whooley, MA, de Jonge, P, Vittinghoff, E, Otte, C, Moos, R, Carney, RM, Ali, S, Dowray, S, Na, B, Feldman, MD, Schiller, NB, Browner, WS (2008). Depressive symptoms, health behaviors, and risk of cardiovascular events in patients with coronary heart disease. JAMA 300, 2379–2388.Google Scholar
Yanbaeva, DG, Dentener, MA, Creutzberg, EC, Wesseling, G, Wouters, EF (2007). Systemic effects of smoking. Chest 131, 1557–1566.Google Scholar
Yoon, HK, Kim, YK, Lee, HJ, Kwon, DY, Kim, L (2012). Role of cytokines in atypical depression. Nordic Journal of Psychiatry 66, 183–188.Google Scholar