Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-05T08:13:01.411Z Has data issue: false hasContentIssue false
  • English
  • Français

Endothelial dysfunction is associated with a greater depressive symptom score in a general elderly population: the Hoorn Study

Published online by Cambridge University Press:  13 August 2013

T. T. van Sloten ,
M. T. Schram ,
M. C. Adriaanse ,
J. M. Dekker ,
G. Nijpels ,
T. Teerlink ,
P. G. Scheffer ,
F. Pouwer ,
C. G. Schalkwijk  and
C. D. A. Stehouwer
...Show all authors
T. T. van Sloten
Affiliation:
Department of Medicine, Maastricht University Medical Centre, The Netherlands Cardiovascular Research Institute Maastricht, Maastricht University Medical Centre, The Netherlands School for Nutrition, Toxicology and Metabolism, Maastricht University Medical Centre, The Netherlands
M. T. Schram
Affiliation:
Department of Medicine, Maastricht University Medical Centre, The Netherlands Cardiovascular Research Institute Maastricht, Maastricht University Medical Centre, The Netherlands
M. C. Adriaanse
Affiliation:
EMGO Institute for Health and Care Research, VU University Medical Centre, Amsterdam, The Netherlands
J. M. Dekker
Affiliation:
EMGO Institute for Health and Care Research, VU University Medical Centre, Amsterdam, The Netherlands Department of Epidemiology and Biostatistics, VU University Medical Centre, Amsterdam, The Netherlands
G. Nijpels
Affiliation:
EMGO Institute for Health and Care Research, VU University Medical Centre, Amsterdam, The Netherlands
T. Teerlink
Affiliation:
Metabolic Laboratory, Department of Clinical Chemistry, VU University Medical Centre, Amsterdam, The Netherlands
P. G. Scheffer
Affiliation:
Metabolic Laboratory, Department of Clinical Chemistry, VU University Medical Centre, Amsterdam, The Netherlands
F. Pouwer
Affiliation:
Centre of Research on Psychology in Somatic Diseases, Department of Medical Psychology and Neuropsychology, Tilburg University, The Netherlands
C. G. Schalkwijk
Affiliation:
Department of Medicine, Maastricht University Medical Centre, The Netherlands Cardiovascular Research Institute Maastricht, Maastricht University Medical Centre, The Netherlands
C. D. A. Stehouwer
Affiliation:
Department of Medicine, Maastricht University Medical Centre, The Netherlands Cardiovascular Research Institute Maastricht, Maastricht University Medical Centre, The Netherlands School for Nutrition, Toxicology and Metabolism, Maastricht University Medical Centre, The Netherlands
R. M. A. Henry*
Affiliation:
Department of Medicine, Maastricht University Medical Centre, The Netherlands Cardiovascular Research Institute Maastricht, Maastricht University Medical Centre, The Netherlands
*
* Address for correspondence: R. M. A. Henry, Ph.D., M.D., Department of Medicine, Maastricht University Medical Centre, Prof. Debyelaan 25, 6229 HX Maastricht, The Netherlands. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Endothelial dysfunction (ED), low-grade inflammation (LGI) and oxidative stress (OxS) may be involved in the pathobiology of depression. Previous studies on the association of these processes in depression have yielded contradictory results. We therefore investigated comprehensively, in a population-based cohort study, the association between ED, LGI and OxS on the one hand and depressive symptoms on the other.

Method

We used data from the Hoorn Study and determined biomarkers of ED [flow-mediated dilatation (FMD), von Willebrand factor, soluble intercellular adhesion molecule 1 (sICAM-1), soluble vascular cell adhesion molecule 1, soluble thrombomodulin and soluble endothelial selectin], LGI [C-reactive protein, tumour necrosis factor-α, interleukin 6, interleukin 8, serum amyloid A, myeloperoxidase (MPO) and sICAM-1] and OxS (oxidized low density lipoprotein and MPO). Depressive symptoms were quantified by the Center for Epidemiologic Studies Depression Scale (CES-D) questionnaire (n = 493; age 68 years; 49.9% female). Regression analyses were performed with the use of biomarker Z scores. Adjustments were made for age, sex and glucose metabolism status (cohort stratification variables) and prior cardiovascular disease, hypertension, waist-to-hip ratio, cholesterol levels, education level, physical activity, dietary habits, and the use of antihypertensive and/or lipid-lowering medication and/or metformin (potential confounders).

Results

After adjustment for age, sex and glucose metabolism status, one standard deviation increase in the ED Z score was associated with a 1.9 [95% confidence interval (CI) 0.7–3.1] higher CES-D score. Additional adjustments did not materially change this result. LGI and OxS were not associated with the CES-D score.

Conclusions

ED, as quantified by an array of circulating biomarkers and FMD, was independently associated with depressive symptoms. This study supports the hypothesis that ED plays an important role in the pathobiology of depression.

Keywords

Depressionendothelial dysfunctionlow-grade inflammationoxidative stress
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 7 , May 2014 , pp. 1403 - 1416
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aird, WC (2007 a). Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circulation Research 100, 158–173.CrossRefGoogle ScholarPubMed
Aird, WC (2007 b). Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circulation Research 100, 174–190.CrossRefGoogle ScholarPubMed
Beekman, AT, Deeg, DJ, Van Limbeek, J, Braam, AW, De Vries, MZ, Van Tilburg, W (1997). Criterion validity of the Center for Epidemiologic Studies Depression scale (CES-D): results from a community-based sample of older subjects in The Netherlands. Psychological Medicine 27, 231–235.CrossRefGoogle Scholar
Belmaker, RH, Agam, G (2008). Major depressive disorder. New England Journal of Medicine 358, 55–68.CrossRefGoogle ScholarPubMed
Brennan, ML, Penn, MS, Van Lente, F, Nambi, V, Shishehbor, MH, Aviles, RJ, Goormastic, M, Pepoy, ML, McErlean, ES, Topol, EJ, Nissen, SE, Hazen, SL (2003). Prognostic value of myeloperoxidase in patients with chest pain. New England Journal of Medicine 349, 1595–1604.CrossRefGoogle ScholarPubMed
Brevetti, G, Martone, VD, de Cristofaro, T, Corrado, S, Silvestro, A, Di Donato, AM, Bucur, R, Scopacasa, F (2001). High levels of adhesion molecules are associated with impaired endothelium-dependent vasodilation in patients with peripheral arterial disease. Thrombosis and Haemostasis 85, 63–66.Google ScholarPubMed
Broadley, AJ, Korszun, A, Abdelaal, E, Moskvina, V, Deanfield, J, Jones, CJ, Frenneaux, MP (2006). Metyrapone improves endothelial dysfunction in patients with treated depression. Journal of the American College of Cardiology 48, 170–175.CrossRefGoogle ScholarPubMed
Cooper, DC, Milic, MS, Tafur, JR, Mills, PJ, Bardwell, WA, Ziegler, MG, Dimsdale, JE (2010). Adverse impact of mood on flow-mediated dilation. Psychosomatic Medicine 72, 122–127.CrossRefGoogle ScholarPubMed
Corretti, MC, Anderson, TJ, Benjamin, EJ, Celermajer, D, Charbonneau, F, Creager, MA, Deanfield, J, Drexler, H, Gerhard-Herman, M, Herrington, D, Vallance, P, Vita, J, Vogel, R (2002). Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. Journal of the American College of Cardiology 39, 257–265.CrossRefGoogle ScholarPubMed
Dantzer, R, O'Connor, JC, Freund, GG, Johnson, RW, Kelley, KW (2008). From inflammation to sickness and depression: when the immune system subjugates the brain. Nature Reviews Neuroscience 9, 46–56.CrossRefGoogle ScholarPubMed
Direk, N, Koudstaal, PJ, Hofman, A, Ikram, MA, Hoogendijk, WJ, Tiemeier, H (2012). Cerebral hemodynamics and incident depression: the Rotterdam Study. Biological Psychiatry 72, 318–323.CrossRefGoogle ScholarPubMed
Do, DP, Dowd, JB, Ranjit, N, House, JS, Kaplan, GA (2010). Hopelessness, depression, and early markers of endothelial dysfunction in U.S. adults. Psychosomatic Medicine 72, 613–619.CrossRefGoogle ScholarPubMed
Du, H, van der A, DL, van Bakel, MM, van der Kallen, CJ, Blaak, EE, van Greevenbroek, MM, Jansen, EH, Nijpels, G, Stehouwer, CD, Dekker, JM, Feskens, EJ (2008). Glycemic index and glycemic load in relation to food and nutrient intake and metabolic risk factors in a Dutch population. American Journal of Clinical Nutrition 87, 655–661.CrossRefGoogle Scholar
Elovainio, M, Aalto, AM, Kivimaki, M, Pirkola, S, Sundvall, J, Lonnqvist, J, Reunanen, A (2009). Depression and C-reactive protein: population-based Health 2000 Study. Psychosomatic Medicine 71, 423–430.CrossRefGoogle ScholarPubMed
Empana, JP, Sykes, DH, Luc, G, Juhan-Vague, I, Arveiler, D, Ferrieres, J, Amouyel, P, Bingham, A, Montaye, M, Ruidavets, JB, Haas, B, Evans, A, Jouven, X, Ducimetiere, P (2005). Contributions of depressive mood and circulating inflammatory markers to coronary heart disease in healthy European men: the Prospective Epidemiological Study of Myocardial Infarction (PRIME). Circulation 111, 2299–2305.CrossRefGoogle ScholarPubMed
Ford, DE, Erlinger, TP (2004). Depression and C-reactive protein in US adults: data from the Third National Health and Nutrition Examination Survey. Archives of Internal Medicine 164, 1010–1014.CrossRefGoogle ScholarPubMed
Forlenza, MJ, Miller, GE (2006). Increased serum levels of 8-hydroxy-2′-deoxyguanosine in clinical depression. Psychosomatic Medicine 68, 1–7.CrossRefGoogle ScholarPubMed
Fung, TT, McCullough, ML, Newby, PK, Manson, JE, Meigs, JB, Rifai, N, Willett, WC, Hu, FB (2005). Diet-quality scores and plasma concentrations of markers of inflammation and endothelial dysfunction. American Journal of Clinical Nutrition 82, 163–173.CrossRefGoogle Scholar
Henry, RM, Ferreira, I, Kostense, PJ, Dekker, JM, Nijpels, G, Heine, RJ, Kamp, O, Bouter, LM, Stehouwer, CD (2004). Type 2 diabetes is associated with impaired endothelium-dependent, flow-mediated dilation, but impaired glucose metabolism is not – the Hoorn Study. Atherosclerosis 174, 49–56.CrossRefGoogle Scholar
Henry, RM, Kostense, PJ, Spijkerman, AM, Dekker, JM, Nijpels, G, Heine, RJ, Kamp, O, Westerhof, N, Bouter, LM, Stehouwer, CD (2003). Arterial stiffness increases with deteriorating glucose tolerance status: the Hoorn Study. Circulation 107, 2089–2095.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Jager, A, van Hinsbergh, VW, Kostense, PJ, Emeis, JJ, Yudkin, JS, Nijpels, G, Dekker, JM, Heine, RJ, Bouter, LM, Stehouwer, CD (1999). von Willebrand factor, C-reactive protein, and 5-year mortality in diabetic and nondiabetic subjects: the Hoorn Study. Arteriosclerosis, Thrombosis, and Vascular Biology 19, 3071–3078.CrossRefGoogle ScholarPubMed
Krishnan, V, Nestler, EJ (2010). Linking molecules to mood: new insight into the biology of depression. American Journal of Psychiatry 167, 1305–1320.CrossRefGoogle ScholarPubMed
Kupper, N, Gidron, Y, Winter, J, Denollet, J (2009). Association between type D personality, depression, and oxidative stress in patients with chronic heart failure. Psychosomatic Medicine 71, 973–980.CrossRefGoogle ScholarPubMed
Lemke, H, de Castro, AG, Schlattmann, P, Heuser, I, Neu, P (2010). Cerebrovascular reactivity over time-course – from major depressive episode to remission. Journal of Psychiatric Research 44, 132–136.CrossRefGoogle ScholarPubMed
Lesperance, F, Frasure-Smith, N, Theroux, P, Irwin, M (2004). The association between major depression and levels of soluble intercellular adhesion molecule 1, interleukin-6, and C-reactive protein in patients with recent acute coronary syndromes. American Journal of Psychiatry 161, 271–277.CrossRefGoogle ScholarPubMed
Levey, AS, Coresh, J, Greene, T, Marsh, J, Stevens, LA, Kusek, JW, Van Lente, F (2007). Expressing the Modification of Diet in Renal Disease Study equation for estimating glomerular filtration rate with standardized serum creatinine values. Clinical Chemistry 53, 766–772.CrossRefGoogle ScholarPubMed
Maes, M, Galecki, P, Chang, YS, Berk, M (2011). A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Progress in Neuro-Psychopharmacology and Biological Psychiatry 35, 676–692.CrossRefGoogle Scholar
Maes, M, Mihaylova, I, Kubera, M, Uytterhoeven, M, Vrydags, N, Bosmans, E (2010). Increased plasma peroxides and serum oxidized low density lipoprotein antibodies in major depression: markers that further explain the higher incidence of neurodegeneration and coronary artery disease. Journal of Affective Disorders 125, 287–294.CrossRefGoogle ScholarPubMed
Miller, AH, Maletic, V, Raison, CL (2009). Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biological Psychiatry 65, 732–741.CrossRefGoogle ScholarPubMed
Mooy, JM, Grootenhuis, PA, de Vries, H, Valkenburg, HA, Bouter, LM, Kostense, PJ, Heine, RJ (1995). Prevalence and determinants of glucose intolerance in a Dutch Caucasian population. The Hoorn Study. Diabetes Care 18, 1270–1273.CrossRefGoogle Scholar
Musselman, DL, Betan, E, Larsen, H, Phillips, LS (2003). Relationship of depression to diabetes types 1 and 2: epidemiology, biology, and treatment. Biological Psychiatry 54, 317–329.CrossRefGoogle ScholarPubMed
Narita, K, Murata, T, Hamada, T, Takahashi, T, Omori, M, Suganuma, N, Yoshida, H, Wada, Y (2007). Interactions among higher trait anxiety, sympathetic activity, and endothelial function in the elderly. Journal of Psychiatric Research 41, 418–427.CrossRefGoogle ScholarPubMed
Ocke, MC, Bueno-de-Mesquita, HB, Goddijn, HE, Jansen, A, Pols, MA, van Staveren, WA, Kromhout, D (1997 a). The Dutch EPIC Food Frequency Questionnaire. I. Description of the questionnaire, and relative validity and reproducibility for food groups. International Journal of Epidemiology 26 (Suppl. 1), S37–S48.CrossRefGoogle ScholarPubMed
Ocke, MC, Bueno-de-Mesquita, HB, Pols, MA, Smit, HA, van Staveren, WA, Kromhout, D (1997 b). The Dutch EPIC Food Frequency Questionnaire. II. Relative validity and reproducibility for nutrients. International Journal of Epidemiology 26 (Suppl. 1), S49–S58.CrossRefGoogle ScholarPubMed
Panagiotakos, DB, Pitsavos, C, Chrysohoou, C, Tsetsekou, E, Papageorgiou, C, Christodoulou, G, Stefanadis, C (2004). Inflammation, coagulation, and depressive symptomatology in cardiovascular disease-free people: the ATTICA study. European Heart Journal 25, 492–499.CrossRefGoogle ScholarPubMed
Paranthaman, R, Greenstein, AS, Burns, AS, Cruickshank, JK, Heagerty, AM, Jackson, A, Malik, RA, Scott, ML, Baldwin, RC (2010). Vascular function in older adults with depressive disorder. Biological Psychiatry 68, 133–139.CrossRefGoogle ScholarPubMed
Parker, G, Gibson, NA, Brotchie, H, Heruc, G, Rees, AM, Hadzi-Pavlovic, D (2006). Omega-3 fatty acids and mood disorders. American Journal of Psychiatry 163, 969–978.CrossRefGoogle ScholarPubMed
Penninx, BW, Kritchevsky, SB, Yaffe, K, Newman, AB, Simonsick, EM, Rubin, S, Ferrucci, L, Harris, T, Pahor, M (2003). Inflammatory markers and depressed mood in older persons: results from the Health, Aging and Body Composition study. Biological Psychiatry 54, 566–572.CrossRefGoogle ScholarPubMed
Pizzi, C, Manzoli, L, Mancini, S, Costa, GM (2008). Analysis of potential predictors of depression among coronary heart disease risk factors including heart rate variability, markers of inflammation, and endothelial function. European Heart Journal 29, 1110–1117.CrossRefGoogle Scholar
Ridker, PM, Hennekens, CH, Buring, JE, Rifai, N (2000). C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. New England Journal of Medicine 342, 836–843.CrossRefGoogle Scholar
Rothman, KJ, Greenland, S, Lash, TJ (2008). Modern Epidemiology. Lippincott Williams and Wilkins: Philadelphia, PA.Google Scholar
Rybakowski, JK, Wykretowicz, A, Heymann-Szlachcinska, A, Wysocki, H (2006). Impairment of endothelial function in unipolar and bipolar depression. Biological Psychiatry 60, 889–891.CrossRefGoogle ScholarPubMed
Schindhelm, RK, van der Zwan, LP, Teerlink, T, Scheffer, PG (2009). Myeloperoxidase: a useful biomarker for cardiovascular disease risk stratification? Clinical Chemistry 55, 1462–1470.CrossRefGoogle ScholarPubMed
Schott, LL, Kamarck, TW, Matthews, KA, Brockwell, SE, Sutton-Tyrrell, K (2009). Is brachial artery flow-mediated dilation associated with negative affect? International Journal of Behavioral Medicine 16, 241–247.CrossRefGoogle ScholarPubMed
Schram, MT, Stehouwer, CD (2005). Endothelial dysfunction, cellular adhesion molecules and the metabolic syndrome. Hormone and Metabolic Research 37 (Suppl. 1), 49–55.CrossRefGoogle ScholarPubMed
Selvin, S (1996). Statistical Analysis of Epidemiologic Data. Oxford University Press: New York.Google Scholar
Shen, Q, Goderie, SK, Jin, L, Karanth, N, Sun, Y, Abramova, N, Vincent, P, Pumiglia, K, Temple, S (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338–1340.CrossRefGoogle ScholarPubMed
Sherwood, A, Hinderliter, AL, Watkins, LL, Waugh, RA, Blumenthal, JA (2005). Impaired endothelial function in coronary heart disease patients with depressive symptomatology. Journal of the American College of Cardiology 46, 656–659.CrossRefGoogle ScholarPubMed
Spijkerman, AM, Adriaanse, MC, Dekker, JM, Nijpels, G, Stehouwer, CD, Bouter, LM, Heine, RJ (2002). Diabetic patients detected by population-based stepwise screening already have a diabetic cardiovascular risk profile. Diabetes Care 25, 1784–1789.CrossRefGoogle ScholarPubMed
Stehouwer, CD, Gall, MA, Twisk, JW, Knudsen, E, Emeis, JJ, Parving, HH (2002). Increased urinary albumin excretion, endothelial dysfunction, and chronic low-grade inflammation in type 2 diabetes: progressive, interrelated, and independently associated with risk of death. Diabetes 51, 1157–1165.CrossRefGoogle ScholarPubMed
Thomas, AJ, Morris, C, Davis, S, Jackson, E, Harrison, R, O'Brien, JT (2007). Soluble cell adhesion molecules in late-life depression. International Psychogeriatrics 19, 914–920.CrossRefGoogle ScholarPubMed
Tiemeier, H, Hofman, A, van Tuijl, HR, Kiliaan, AJ, Meijer, J, Breteler, MM (2003). Inflammatory proteins and depression in the elderly. Epidemiology 14, 103–107.CrossRefGoogle ScholarPubMed
Unwin, N, Shaw, J, Zimmet, P, Alberti, KG (2002). Impaired glucose tolerance and impaired fasting glycaemia: the current status on definition and intervention. Diabetic Medicine 19, 708–723.Google ScholarPubMed
van Bussel, BC, Henry, RM, Schalkwijk, CG, Ferreira, I, Feskens, EJ, Streppel, MT, Smulders, YM, Twisk, JW, Stehouwer, CD (2011 a). Fish consumption in healthy adults is associated with decreased circulating biomarkers of endothelial dysfunction and inflammation during a 6-year follow-up. Journal of Nutrition 141, 1719–1725.CrossRefGoogle Scholar
van Bussel, BC, Schouten, F, Henry, RM, Schalkwijk, CG, de Boer, MR, Ferreira, I, Smulders, YM, Twisk, JW, Stehouwer, CD (2011 b). Endothelial dysfunction and low-grade inflammation are associated with greater arterial stiffness over a 6-year period. Hypertension 58, 588–595.CrossRefGoogle Scholar
Van der Zwan, LP, Scheffer, PG, Dekker, JM, Stehouwer, CD, Heine, RJ, Teerlink, T (2010 a). Hyperglycemia and oxidative stress strengthen the association between myeloperoxidase and blood pressure. Hypertension 55, 1366–1372.CrossRefGoogle ScholarPubMed
van der Zwan, LP, Teerlink, T, Dekker, JM, Henry, RM, Stehouwer, CD, Jakobs, C, Heine, RJ, Scheffer, PG (2009). Circulating oxidized LDL: determinants and association with brachial flow-mediated dilation. Journal of Lipid Research 50, 342–349.CrossRefGoogle ScholarPubMed
van der Zwan, LP, Teerlink, T, Dekker, JM, Henry, RM, Stehouwer, CD, Jakobs, C, Heine, RJ, Scheffer, PG (2010 b). Plasma myeloperoxidase is inversely associated with endothelium-dependent vasodilation in elderly subjects with abnormal glucose metabolism. Metabolism 59, 1723–1729.CrossRefGoogle ScholarPubMed
Wendel-Vos, GC, Schuit, AJ, Saris, WH, Kromhout, D (2003). Reproducibility and relative validity of the Short Questionnaire to Assess Health-enhancing physical activity. Journal of Clinical Epidemiology 56, 1163–1169.CrossRefGoogle ScholarPubMed
Wu, KK (2003). Soluble thrombomodulin and coronary heart disease. Current Opinion in Lipidology 14, 373–375.CrossRefGoogle ScholarPubMed
Yudkin, JS, Stehouwer, CD, Emeis, JJ, Coppack, SW (1999). C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arteriosclerosis, Thrombosis, and Vascular Biology 19, 972–978.CrossRefGoogle ScholarPubMed
Zhao, C, Deng, W, Gage, FH (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645–660.CrossRefGoogle ScholarPubMed