Seasonal variation in muscle sympathetic nerve activity

Jian Cui, Matthew D Muller, Cheryl Blaha, Allen R Kunselman, Lawrence I Sinoway, Jian Cui, Matthew D Muller, Cheryl Blaha, Allen R Kunselman, Lawrence I Sinoway

Abstract

Epidemiologic data suggest there are seasonal variations in the incidence of severe cardiac events with peak levels being evident in the winter. Whether autonomic indices including muscle sympathetic nerve activity (MSNA) vary with season remains unclear. In this report, we tested the hypothesis that resting MSNA varies with the seasons of the year with peak levels evident in the winter. We analyzed the supine resting MSNA in 60 healthy subjects. Each subject was studied during two, three, or four seasons (total 237 visits). MSNA burst rate in the winter (21.0 ± 6.8 burst/min, mean ± SD) was significantly greater than in the summer (13.5 ± 5.8 burst/min, P < 0.001), the spring (17.1 ± 9.0 burst/min, P = 0.03), and the fall (17.9 ± 7.7 burst/min, P = 0.002). There was no significant difference in MSNA for other seasonal comparisons. The results suggest that resting sympathetic nerve activity varies along the seasons, with peak levels evident in the winter. We speculate that the seasonal changes in sympathetic activity may be a contribution to the previously observed seasonal variations in cardiovascular morbidity and mortality.

Keywords: Cardiovascular diseases; hemodynamic; nervous system; risk factors; sympathetic.

© 2015 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of the American Physiological Society and The Physiological Society.

Figures

Figure 1
Figure 1
Heart rate (HR), mean arterial blood pressure (MAP), MSNA burst rate (right upper panel), and MSNA burst incidence (right lower panel) in the four seasons. Data are reported as means ± SD. Subject numbers for each season are reported in Table1. Unadjusted P value for the seasons: = 0.109 for HR, = 0.656 for MAP, < 0.001 for MSNA burst rate, and < 0.001 for MSNA burst incidence. After adjusting for gender, age, and BMI, = 0.117 for HR, = 0.652 for MAP, < 0.001 for MSNA burst rate, and < 0.001 for MSNA burst incidence. P values in the figure (e.g., = 0.027/0.009) were the unadjusted value and the adjusted value for gender, age, and BMI, respectively.
Figure 2
Figure 2
Systolic (SBP) and diastolic (DBP) blood pressure in the four seasons. Subject numbers for each season are reported in Table1. Unadjusted P value for the seasons: = 0.043 for SBP and = 0.286 for DBP. After adjusting for gender, age, and BMI, = 0.056 for SBP and = 0.264 for DBP.
Figure 3
Figure 3
Relationships within MAP, HR, and MSNA between the winter and other three seasons. Each dot in the graphs represents the variable observed in two seasons in an individual subject. The subjects for each comparison of the seasons were the same. The subgroups of the subjects in the upper, middle, and lower panels were not the exact same, but had overlap. = 19 for winter to spring. = 25 for winter to summer. = 28 for winter to fall.

References

    1. Alperovitch A, Lacombe JM, Hanon O, Dartigues JF, Ritchie K, Ducimetiere P, et al. Relationship between blood pressure and outdoor temperature in a large sample of elderly individuals: the Three-City study. Arch. Intern. Med. 2009;169:75–80.
    1. Ballaro A, Cortina-Borja M. Collin J. A seasonal variation in the incidence of ruptured abdominal aortic aneurysms. Eur. J. Vasc. Endovasc. Surg. 1998;15:429–431.
    1. Barnett AG, Sans S, Salomaa V, Kuulasmaa K, Dobson AJ. Project WM. The effect of temperature on systolic blood pressure. Blood Press. Monit. 2007;12:195–203.
    1. Barretto AC, Santos AC, Munhoz R, Rondon MU, Franco FG, Trombetta IC, et al. Increased muscle sympathetic nerve activity predicts mortality in heart failure patients. Int. J. Cardiol. 2009;135:302–307.
    1. Boulay F, Berthier F, Sisteron O, Gendreike Y. Gibelin P. Seasonal variation in chronic heart failure hospitalizations and mortality in France. Circulation. 1999;100:280–286.
    1. Brennan PJ, Greenberg G, Miall WE. Thompson SG. Seasonal variation in arterial blood pressure. Br. Med. J. (Clin Res Ed) 1982;285:919–923. PMCID: PMC1499985.
    1. Carter JR, Lawrence JE. Klein JC. Menstrual cycle alters sympathetic neural responses to orthostatic stress in young, eumenorrheic women. Am. J. Physiol. Endocrinol. Metab. 2009;297:E85–E91. PMCID: PMC2711656.
    1. Cohn JN, Levine TB, Olivari MT, Garberg V, Lura D, Francis GS, et al. Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure. N. Engl. J. Med. 1984;311:819–823.
    1. Cui J, Blaha C, Moradkhan M, Gray K. Sinoway L. Muscle sympathetic nerve activity responses to dynamic passive muscle stretch in humans. J. Physiol. 2006;576:625–634. PMCID: PMC1890351.
    1. Cui J, McQuillan P, Momen A, Blaha C, Moradkhan R, Mascarenhas V, et al. The role of the cyclooxygenase products in evoking sympathetic activation in exercise. Am. J. Physiol. Heart Circ. Physiol. 2007;293:H1861–H1868. PMCID: PMC2559802.
    1. Cui J, Mascarenhas V, Moradkhan R, Blaha C. Sinoway LI. Effects of muscle metabolites on responses of muscle sympathetic nerve activity to mechanoreceptor(s) stimulation in healthy humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008a;294:R458–R466.
    1. Cui J, Moradkhan R, Mascarenhas V, Momen A. Sinoway L. Cyclooxygenase inhibition attenuates sympathetic responses to muscle stretch in humans. Am. J. Physiol. Heart Circ. Physiol. 2008b;294:H2693–H2700. PMCID: PMC3531047.
    1. Cui J, McQuillan P, Moradkhan R, Pagana C. Sinoway LI. Sympathetic responses during saline infusion into the veins of an occluded limb. J. Physiol. 2009;587:3619–3628. PMCID: PMC2742285.
    1. Cui J, Leuenberger UA, Blaha C, Yoder J, Gao Z. Sinoway LI. Local adenosine receptor blockade accentuates the sympathetic responses to fatiguing exercise. Am. J. Physiol. Heart Circ. Physiol. 2010;298:H2130–H2137. PMCID: PMC2886659.
    1. Cui J, Leuenberger UA, Blaha C, King NC. Sinoway LI. Effect of P2 receptor blockade with pyridoxine on sympathetic response to exercise pressor reflex in humans. J. Physiol. 2011a;589:685–695. PMCID: PMC3055551.
    1. Cui J, Leuenberger UA, Gao Z. Sinoway LI. Sympathetic and cardiovascular responses to venous distension in an occluded limb. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011b;301:R1831–R1837. PMCID: PMC3233857.
    1. Cui J, Blaha C, Herr M, Mast J, Muller M, Drew R, et al. Negative pressure on an occluded limb induces sympathetic activation. FASEB J. 2012a;26 1091.1 (Abstract)
    1. Cui J, McQuillan P, Blaha CA, Kunselman AR. Sinoway LI. Limb venous distension evokes sympathetic activation via stimulation of the limb afferents in humans. Am. J. Physiol. Heart Circ. Physiol. 2012b;303:H457–H463. PMCID: PMC3423143.
    1. Cui J, Gao Z, Blaha C, Herr MD, Mast J. Sinoway LI. Distension of central great vein decreases sympathetic outflow in humans. Am. J. Physiol. Heart Circ. Physiol. 2013;305:H378–H385. PMCID: PMC3742879.
    1. Dannenberg AL, Keller JB, Wilson PW. Castelli WP. Leisure time physical activity in the Framingham Offspring Study. Description, seasonal variation, and risk factor correlates. Am. J. Epidemiol. 1989;129:76–88.
    1. Diaz A, Ferrante D, Badra R, Morales I, Becerra A, Varini S, et al. Seasonal variation and trends in heart failure morbidity and mortality in a South American community hospital. Congest. Heart Fail. 2007;13:263–266.
    1. Dunnigan MG, Harland WA. Fyfe T. Seasonal incidence and mortality of ischaemic heart-disease. Lancet. 1970;2:793–797.
    1. Evans JM, Ziegler MG, Patwardhan AR, Ott JB, Kim CS, Leonelli FM, et al. Gender differences in autonomic cardiovascular regulation: spectral, hormonal, and hemodynamic indexes. J. Appl. Physiol. (1985) 2001;91:2611–2618.
    1. Fagius J. Wallin BG. Long-term variability and reproducibility of resting human muscle nerve sympathetic activity at rest, as reassessed after a decade. Clin. Auton. Res. 1993;3:201–205.
    1. Furlan R, Porta A, Costa F, Tank J, Baker L, Schiavi R, et al. Oscillatory patterns in sympathetic neural discharge and cardiovascular variables during orthostatic stimulus. Circulation. 2000;101:886–892.
    1. Grassi G, Seravalle G, Quarti-Trevano F, Dell’Oro R, Bolla G. Mancia G. Effects of hypertension and obesity on the sympathetic activation of heart failure patients. Hypertension. 2003;42:873–877.
    1. Halliwill JR. Segregated signal averaging of sympathetic baroreflex responses in humans. J. Appl. Physiol. 2000;88:767–773.
    1. Halonen JI, Zanobetti A, Sparrow D, Vokonas PS. Schwartz J. Relationship between outdoor temperature and blood pressure. Occup. Environ. Med. 2011;68:296–301.
    1. Hess KL, Wilson TE, Sauder CL, Gao Z, Ray CA. Monahan KD. Aging affects the cardiovascular responses to cold stress in humans. J. Appl. Physiol. 2009;107:1076–1082. PMCID: PMC2763834.
    1. Hoffman RP, Sinkey CA. Anderson EA. Microneurographically determined muscle sympathetic nerve activity levels are reproducible in insulin-dependent diabetes mellitus. J. Diabetes Complications. 1998;12:307–310.
    1. Hopstock LA, Barnett AG, Bonaa KH, Mannsverk J, Njolstad I. Wilsgaard T. Seasonal variation in cardiovascular disease risk factors in a subarctic population: the Tromso Study 1979–2008. J. Epidemiol. Community Health. 2013;67:113–118.
    1. Izzo JL, Jr, Larrabee PS, Sander E. Lillis LM. Hemodynamics of seasonal adaptation. Am. J. Hypertens. 1990;3:405–407.
    1. Jarvis SS, VanGundy TB, Galbreath MM, Shibata S, Okazaki K, Reelick MF, et al. Sex differences in the modulation of vasomotor sympathetic outflow during static handgrip exercise in healthy young humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011;301:R193–R200. PMCID: PMC3129874.
    1. Kasper S, Wehr TA, Bartko JJ, Gaist PA. Rosenthal NE. Epidemiological findings of seasonal changes in mood and behavior. A telephone survey of Montgomery County, Maryland. Arch. Gen. Psychiatry. 1989;46:823–833.
    1. Kent ST, Howard G, Crosson WL, Prineas RJ. McClure LA. The association of remotely-sensed outdoor temperature with blood pressure levels in REGARDS: a cross-sectional study of a large, national cohort of African-American and white participants. Environ. Health. 2011;10:7. PMCID: PMC3032648.
    1. Kloner RA, Poole WK. Perritt RL. When throughout the year is coronary death most likely to occur? A 12-year population-based analysis of more than 220,000 cases. Circulation. 1999;100:1630–1634.
    1. Kristal-Boneh E, Froom P, Harari G, Malik M. Ribak J. Summer-winter differences in 24 h variability of heart rate. J. Cardiovasc. Risk. 2000;7:141–146.
    1. Martinez-Selles M, Garcia Robles JA, Prieto L, Serrano JA, Munoz R, Frades E, et al. Annual rates of admission and seasonal variations in hospitalizations for heart failure. Eur. J. Heart Fail. 2002;4:779–786.
    1. Mehta RH, Manfredini R, Hassan F, Sechtem U, Bossone E, Oh JK, et al. International Registry of Acute Aortic Dissection Investigators. Chronobiological patterns of acute aortic dissection. Circulation. 2002;106:1110–1115.
    1. Middlekauff HR. Sontz EM. Morning sympathetic nerve activity is not increased in humans. Implications for mechanisms underlying the circadian pattern of cardiac risk. Circulation. 1995;91:2549–2555.
    1. Minson CT, Halliwill JR, Young TM. Joyner MJ. Influence of the menstrual cycle on sympathetic activity, baroreflex sensitivity, and vascular transduction in young women. Circulation. 2000;101:862–868.
    1. Modesti PA, Morabito M, Massetti L, Rapi S, Orlandini S, Mancia G, et al. Seasonal blood pressure changes: an independent relationship with temperature and daylight hours. Hypertension. 2013;61:908–914.
    1. Ng AV, Callister R, Johnson DG. Seals DR. Age and gender influence muscle sympathetic nerve activity at rest in healthy humans. Hypertension. 1993;21:498–503.
    1. Niimi Y, Matsukawa T, Sugiyama Y, Shamsuzzaman AS. Mano T. Comparison [correction of Compariso] of sympathetic nerve response to head-up tilt in summer [correction of sumer] and winter. J. Gravit. Physiol. 1999;6:P43–P44.
    1. Nyquist PA, Wiebers RD, Jr, Brown DO, Crowson CS. O’Fallon WM. Circadian and seasonal occurrence of subarachnoid and intracerebral hemorrhage. Neurology. 2001;56:190–193.
    1. Packer M. Neurohormonal interactions and adaptations in congestive heart failure. Circulation. 1988;77:721–730.
    1. Radke KJ. Izzo JL., Jr Seasonal variation in haemodynamics and blood pressure-regulating hormones. J. Hum. Hypertens. 2010;24:410–416.
    1. Scherrer U, Randin D, Tappy L, Vollenweider P, Jéquier E. Nicod P. Body fat and sympathetic nerve activity in healthy subjects. Circulation. 1994;89:2634–2640.
    1. Semenza JC, Rubin CH, Falter KH, Selanikio JD, Flanders WD, Howe HL, et al. Heat-related deaths during the July 1995 heat wave in Chicago. N. Engl. J. Med. 1996;335:84–90.
    1. Sheth T, Nair C, Muller J. Yusuf S. Increased winter mortality from acute myocardial infarction and stroke: the effect of age. J. Am. Coll. Cardiol. 1999;33:1916–1919.
    1. Spencer FA, Goldberg RJ, Becker RC. Gore JM. Seasonal distribution of acute myocardial infarction in the second National Registry of Myocardial Infarction. J. Am. Coll. Cardiol. 1998;31:1226–1233.
    1. Stewart S, McIntyre K, Capewell S. McMurray JJ. Heart failure in a cold climate. Seasonal variation in heart failure-related morbidity and mortality. J. Am. Coll. Cardiol. 2002;39:760–766.
    1. Usselman CW, Gimon TI, Nielson CA, Luchyshyn TA, Coverdale NS, Van Uum SH, et al. Menstrual cycle and sex effects on sympathetic responses to acute chemoreflex stress. Am. J. Physiol. Heart Circ. Physiol. 2015;308:H664–H671. PMCID: PMC4360053.
    1. Vallbo AB, Hagbarth K-E, Torebjörk HE. Wallin BG. Somatosensory, proprioceptive and sympathetic activity in human peripheral nerves. Physiol. Rev. 1979;59:919–957.
    1. Verbeke G. Molenberghs G. Linear mixed models for longitudinal data. New York: Springer; 2000.
    1. Victor RG, Seals WN, Jr, Leimbach DR, Wallin BG. Mark AL. Effects of the cold pressor test on muscle sympathetic nerve activity in humans. Hypertension. 1987;9:429–436.
    1. Wallin BG. Interindividual differences in muscle sympathetic nerve activity: a key to new insight into cardiovascular regulation? Acta Physiol. (Oxf) 2007;190:265–275.
    1. Wallin BG. Elam M. Insights from intraneural recordings of sympathetic nerve traffic in humans. News Physiol. Sci. 1994;9:203–207.
    1. Wallin BG, Kunimoto MM. Sellgren J. Possible genetic influence on the strength of human muscle nerve sympathetic activity at rest. Hypertension. 1993;22:282–284.
    1. Woodhouse PR, Khaw KT. Plummer M. Seasonal variation of blood pressure and its relationship to ambient temperature in an elderly population. J. Hypertens. 1993;11:1267–1274.

Source: PubMed

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