Abstract
We tested the hypothesis that acute inflammation may cause arterial stiffening in older adults. We further explored if high cardiorespiratory fitness may partially prevent the unfavorable effect of arterial stiffening produced by acute systemic inflammation in older adults. Using a randomized double-blind sham placebo-controlled design, forty healthy older adults were assigned to receive either an influenza vaccine or a sham vaccine. C-reactive protein and interleukin 6 (IL-6) were measured as markers of inflammation. Carotid-femoral pulse wave velocity (PWV) and augmentation index (AIX) as indices of arterial stiffness and wave reflection were assessed at baseline and 24 and 48 h after each vaccination. When compared with sham placebo, the influenza vaccination caused a significant increase in CRP (p < 0.05) and IL-6 (p < 0.05). Carotid-femoral PWV, but not AIX was significantly increased after influenza vaccination (p < 0.05), but not sham vaccination. The high cardiorespiratory fitness group had an attenuated increase in PWV as compared to the low cardiorespiratory fitness group after acute inflammation (p < 0.05). These findings show that acute inflammation may cause significant increases in arterial stiffness in older adults, but these increases were attenuated in the high cardiorespiratory fitness group as compared to the low cardiorespiratory fitness group.
Similar content being viewed by others
References
Antoniades C, Cunnington C, Antonopoulos A, Neville M, Margaritis M, Demosthenous M, Bendall J, Hale A, Cerrato R, Tousoulis D, Bakogiannis C, Marinou K, Toutouza M, Vlachopoulos C, Leeson P, Stefanadis C, Karpe F, Channon KM (2011) Induction of vascular GTP-cyclohydrolase I and endogenous tetrahydrobiopterin synthesis protect against inflammation-induced endothelial dysfunction in human atherosclerosis. Circulation 124:1860–1870
Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, Forman D, Franklin B, Guazzi M, Gulati M, Keteyian SJ, Lavie CJ, Macko R, Mancini D, Milani RV (2010) American Heart Association Exercise, Cardiac Rehabilitation, and Prevention Committee of the Council on Clinical Cardiology; Council on Epidemiology and Prevention; Council on Peripheral Vascular Disease; Interdisciplinary Council on Quality of Care and Outcomes Research Clinician’s Guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation 122:191–225
Gurven M, Kaplan H, Winking J, Eid Rodriguez D, Vasunilashorn S, Kim JK, Finch C, Crimmins E (2009) Inflammation and infection do not promote arterial aging and cardiovascular disease risk factors among lean horticulturalists. PLoS One 11:e6590
Hein TW, Singh U, Vasquez-Vivar J, Devaraj S, Kuo L, Jialal I (2009) Human C-reactive protein induces endothelial dysfunction and uncoupling of eNOS in vivo. Atherosclerosis 206:61–68
Hingorani AD, Cross J, Kharbanda RK, Mullen MJ, Bhagat K, Taylor M, Donald AE, Palacios M, Griffin GE, Deanfield JE, MacAllister RJ, Vallance P (2000) Acute systemic inflammation impairs endothelium-dependent dilatation in humans. Circulation 102:994–999
Kelly RP, Millasseau SC, Ritter JM, Chowienczyk PJ (2001) Vasoactive drugs influence aortic augmentation index independently of pulse-wave velocity in healthy men. Hypertension 37:1429–1433
Kritchevsky SB, Cesari M, Pahor M (2005) Inflammatory markers and cardiovascular health in older adults. Cardiovasc Res 66:265–275
Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D, Pannier B, Vlachopoulos C, Wilkinson I, Struijker-Boudier H (2006) Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 27:2588–2605
Lee DC, Artero EG, Sui X, Blair SN (2010) Mortality trends in the general population: the importance of cardiorespiratory fitness. J Psychopharmacol 24(4 Suppl):27–35
Libby P (2002) Inflammation in atherosclerosis. Nature 420:868–874
Lind L, Hulthe J, Johansson A, Hedner E (2012) Endotoxin-induced and vaccine-induced systemic inflammation both impair endothelium-dependent vasodilation, but not pulse wave reflection. Vasc Health Risk Manage 8:447–453
Liuba P, Aburawi EH, Pesonen E, Andersson S, Truedsson L, Ylä-Herttuala S, Holmberg L (2007) Residual adverse changes in arterial endothelial function and LDL oxidation after a mild systemic inflammation induced by influenza vaccination. Ann Med 39:392–399
Lowder T, Padgett DA, Woods JA (2005) Moderate exercise protects mice from death due to influenza virus. Brain Behav Immun 19:377–380
Meier CR, Jick SS, Derby LE, Vasilakis C, Jick H (1998) Acute respiratory-tract infections and risk of first-time acute myocardial infarction. Lancet 351:1467–1471
Meyer KC (2005) Aging. Proc Am Thorac Soc 2:433–439
Mitchell GF, Lacourcière Y, Arnold JM, Dunlap ME, Conlin PR, Izzo JL Jr (2005) Changes in aortic stiffness and augmentation index after acute converting enzyme or vasopeptidase inhibition. Hypertension 46:1111–1117
Myers J, Prakash M, Froelicher V, Do D, Partington S, Atwood JE (2002) Exercise capacity and mortality among men referred for exercise testing. N Engl J Med 346:793–801
Park S, Lakatta EG (2012) Role of inflammation in the pathogenesis of arterial stiffness. Yonsei Med J 53:258–261
Pauca AL, O’Rourke MF, Kon ND (2001) Prospective evaluation of a method for estimating ascending aortic pressure from the radial artery pressure waveform. Hypertension 38:932–937
Pierce GL, Donato AJ, LaRocca TJ, Eskurza I, Silver AE, Seals DR (2011) Habitually exercising older men do not demonstrate age-associated vascular endothelial oxidative stress. Aging Cell 10:1032–1037
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. N Engl J Med 342:836–843
Seaberg EC, Benning L, Sharrett AR, Lazar JM, Hodis HN, Mack WJ, Siedner MJ, Phair JP, Kingsley LA, Kaplan RC (2010) Association between human immunodeficiency virus infection and stiffness of the common carotid artery. Stroke 41:2163–2170
Seals DR, Walker AE, Pierce GL, Lesniewski LA (2009) Habitual exercise and vascular ageing. J Physiol 587:5541–5549
Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM (2009) Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 587:3885–3897
Singh U, Devaraj S, Vasquez-Vivar J, Jialal I (2007) C-reactive protein decreases endothelial nitric oxide synthase activity via uncoupling. J Mol Cell Cardiol 43:780–791
Smeeth L, Thomas SL, Hall AJ, Hubbard R, Farrington P, Vallance P (2004) Risk of myocardial infarction and stroke after acute infection or vaccination. N Engl J Med 351:2611–2618
Sui X, LaMonte MJ, Laditka JN, Hardin JW, Chase N, Hooker SP, Blair SN (2007) Cardiorespiratory fitness and adiposity as mortality predictors in older adults. JAMA 298:2507–2516
Tillett HE, Smith JW, Gooch CD (1983) Excess deaths attributable to influenza in England and Wales: age at death and certified cause. Int J Epidemiol 12:344–352
Van Bortel LM, Laurent S, Boutouyrie P, Chowienczyk P, Cruickshank JK, De Backer T, Filipovsky J, Huybrechts S, Mattace-Raso FU, Protogerou AD, Schillaci G, Segers P, Vermeersch S, Weber T (2012) Artery Society; European Society of Hypertension Working Group on Vascular Structure and Function; European Network for Noninvasive Investigation of Large Arteries Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity. J Hypertens 30:445–448
van Bussel BC, Henry RM, Schalkwijk CG, Dekker JM, Nijpels G, Stehouwer CD (2012) Low-grade inflammation, but not endothelial dysfunction, is associated with greater carotid stiffness in the elderly: the Hoorn Study. J Hypertens 30:744–752
Vasunilashorn S, Crimmins EM, Kim JK, Winking J, Gurven M, Kaplan H, Finch CE (2010) Blood lipids, infection, and inflammatory markers in the Tsimane of Bolivia. Am J Hum Biol 22:731–740
Venugopal SK, Devaraj S, Yuhanna P, Shaul P, Jialal I (2002) Demonstration that CRP decreases eNOS expression and bioactivity in human aortic endothelial cells. Circulation 106:1439–1441
Vlachopoulos C, Dima I, Aznaouridis K, Vasiliadou C, Ioakeimidis N, Aggeli C, Toutouza M, Stefanadis C (2005) Acute systemic inflammation increases arterial stiffness and decreases wave reflections in healthy individuals. Circulation 112:2193–2200
Vlachopoulos C, Aznaouridis K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol 30:1318–1327
Vlachopoulos C, Xaplanteris P, Sambatakou H, Mariolis E, Bratsas A, Christoforatou E, Miliou A, Aznaouridis K, Stefanadis C (2011) Acute systemic inflammation induced by influenza A (H1N1) vaccination causes a deterioration in endothelial function in HIV-infected patients. HIV Med 12:594–601
Vyas M, Izzo JL Jr, Lacourcière Y, Arnold JM, Dunlap ME, Amato JL, Pfeffer MA, Mitchell GF (2007) Augmentation index and central aortic stiffness in middle-aged to elderly individuals. Am J Hypertens 20:642–647
Wallace SM, Mäki-Petäjä KM, Cheriyan J, Davidson EH, Cherry L, McEniery CM, Sattar N, Wilkinson IB, Kharbanda RK (2010) Simvastatin prevents inflammation-induced aortic stiffening and endothelial dysfunction. Br J Clin Pharmacol 70:799–806
Wilkinson IB, MacCallum H, Cockcroft JR, Webb DJ (2002) Inhibition of basal nitric oxide synthesis increases aortic augmentation index and pulse wave velocity in vivo. Br J Clin Pharmacol 53:189–192
Wong CM, Lai HK, Ou CQ, Ho SY, Chan KP, Thach TQ, Yang L, Chau YK, Lam TH, Hedley AJ, Peiris JS (2008) Is exercise protective against influenza-associated mortality? PLoS One 3:e2108
Acknowledgments
This work was supported by the Korea Research Foundation Grant funded by the Korean Government (KRF-2009-32A-G00050).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Fabio Fischetti.
Rights and permissions
About this article
Cite this article
Jae, S.Y., Yoon, E.S., Jung, S.J. et al. Effect of cardiorespiratory fitness on acute inflammation induced increases in arterial stiffness in older adults. Eur J Appl Physiol 113, 2159–2166 (2013). https://doi.org/10.1007/s00421-013-2648-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-013-2648-1