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Mechanisms responsible for sympathetic activation by cigarette smoking in humans.
Open accessAbstract
BACKGROUND: The pressor and tachycardic effects of cigarette smoking are associated with an increase in plasma catecholamines, suggesting the dependence of these effects on adrenergic stimulation. Whether the stimulation occurs at a central or a peripheral level and whether reflex mechanisms are involved is unknown. METHODS AND RESULTS: In nine normotensive healthy subjects (age, 33.0 +/- 3.5 years, mean +/- SEM), we measured blood pressure (Finapres device), heart rate (ECG), calf blood flow and vascular resistance (venous occlusion plethysmography), plasma norepinephrine and epinephrine (high-performance liquid chromatography assay), and postganglionic muscle sympathetic nerve activity (microneurography from the peroneal nerve) while subjects were smoking a filter cigarette (nicotine content, 1.1 mg) or were in control condition. Cigarette smoking (which raised plasma nicotine measured by high-performance liquid chromatography from 1.0 +/- 0.9 to 44.2 +/- 7.1 ng/mL) markedly and significantly increased mean arterial pressure (+13.2 +/- 2.3%), heart rate (+30.3 +/- 4.7%), calf vascular resistance (+12.1 +/- 4.9%), plasma norepinephrine (+34.8 +/- 7.0%), and plasma epinephrine (+90.5 +/- 39.0%). In contrast, muscle sympathetic nerve activity showed a marked reduction (integrated activity -31.8 +/- 5.1%, P < .01). The reduction was inversely related to the increase in mean arterial pressure (r = -.67, P < .05), but the slope of the relation was markedly less (-54.1 +/- 7.5%, P < .05) than that obtained by intravenous infusion of phenylephrine in absence of smoking. The hemodynamic and neurohumoral changes were still visible 30 minutes after smoking and occurred again on smoking a second cigarette. Sham smoking was devoid of any hemodynamic and neurohumoral effect. CONCLUSIONS: These data support the hypothesis that in humans the sympathetic activation induced by smoking depends on an increased release and/or a reduced clearance of catecholamines at the neuroeffector junctions. Central sympathetic activity is inhibited by smoking, presumably via a baroreceptor stimulation triggered by the smoking-related pressor response. The baroreflex is impaired by smoking, however, indicating that partial inability to reflexly counteract the effect of sympathetic activation is also responsible for the pressor response.
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“Specifically, nicotine instigates cardiovascular constriction by direct stimulation of epinephrine and norepinephrine release from peripheral sympathetic nerve endings [40].”
From Acute Effects of Nicotine on Physiological and Subjective Sexual Arousal in Nonsmoking Men: A Randomized, Double-Blind, Placebo-Controlled Trial (2008) · cites this paper as [40]
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“The attenuation of physiological sexual arousal following nicotine administration is consistent with literature delineating nicotine’s effects on sympathetic nervous system (SNS) activity.”
From Acute Effects of Nicotine on Physiological and Subjective Sexual Arousal in Nonsmoking Men: A Randomized, Double-Blind, Placebo-Controlled Trial (2008) · cites this paper as [40]
In the citing paper
“These and other studies24,25 indicate that despite the ease of measurement, heart rate cannot be taken as either a marker of cardiac sympathetic adrenergic activity or a reliable indicator of sympathetic activity to other regional circulations.”
From The Sympathetic Nervous System Alterations in Human Hypertension (2015) · cites this paper as [24]
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BackgroundCigarette smoking: an important renal risk factor – far beyond carcinogenesis
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“[159] demonstrated that nicotine increases sympathetic activity via direct stimulation of postganglionic sympathetic nerve endings: smoking a single cigarette markedly increased plasma concentrations of norepinephrine and epinephrine in healthy volunteers, whereas postganglionic muscle sympathetic nerve traffic decrea…”
BackgroundNeuroendocrine and cardiovascular reactions to acute psychological stress are attenuated in smokers
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BackgroundEthnic differences in arterial stiffness and wave reflections after cigarette smoking
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“Smoking for a while, the blood pressure was modified by direct stimulation of postganglionic sympathetic nerve endings Mann et al. 1991; Poulsen et al. 1998), leading to elevated plasma norepinephrine and epinephrine concentrations (Grassi et al. 1994).”
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Microneurography and sympathetic nerve activity: a decade-by-decade journey across 50 years
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“There are several highly cited papers by Grassi and/or Mancia in Tables 2 and 3, many of them in collaboration with one another (Grassi et al. 1994, 1995a, 1998b 200, 2004, 2005).”
BackgroundPathology of the Coronary Arteries in Smokers and Non-Smokers
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“that nicotine activates sympathetic neurotransmission through a direct effect on the central nervous system, by ganglionic stimulation of sympathetic neurotransmission and by facilitating catecholamine release from post-ganglionic nerve endings.(6,7) Moreover, nicotine is believed to participate in tobacco smoke-induc…”
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Not smoking is associated with lower risk of hypertension: results of the Olivetti Heart Study
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Cigarette Smoking Augments Sympathetic Nerve Activity in Patients With Coronary Heart Disease
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“However, there was no positive association between serum cotinine and diastolic BP.”
BackgroundInfluentialChronic Tobacco Exposure by Smoking Develops Insulin Resistance
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“Other results showing increases of plasma catecholamines with smoking [10] provide indirect evidence that the moderate but significant increases of arterial pressure we document in the current study could be associated with increased sympathetic activity, but this is not observable with MSNA recordings due to barorefl…”
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Short-term effect of cigarette smoking on CO2-induced vasomotor reactivity in man
Terborg, C., Bramer, S., Weiller, C., & Röther, J. (2002) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(02)00308-8 · Cited by 39
“Our finding of an elevated MAP in smokers after smoking agrees with several studies, which demonstrate a smoking-induced increase in MAP (and heart rate) associated with sympathetic activation, respectively, catecholamine release [18,55,56,60].”
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Acute Exposure to Diesel Exhaust Increases Muscle Sympathetic Nerve Activity in Humans
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“Moreover, a decrease in baroreflex control has been shown in multiple cardiovascular pathologies, 48 as well as decreased sensitivity after smoking 49 and aging.”
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Neural Circulatory Responses to Carbon Monoxide in Healthy Humans
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Influence of smoking on baroreceptor function
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Sympathetic neural responses to smoking are age dependent
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“For instance, smoking acutely increases BP, and initial studies reported blunted SNS response to cigarette smoking (7); however, the sympathoexcitatory effects of smoking were revealed when the pressor effect of smoking was attenuated by administration of NTP (28).”
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“Exposure to husband smoking increased the risk of hypertension through several mechanisms similar to active smoking, including the stimulation of the sympathetic nervous system induced by impaired baroreflex.(17,35) In addition, they were also found to be associated with elevated levels of inflammation markers and imp…”
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“Pharmacologically, nicotine stimulates the sympathetic nervous system in active smokers.(17) 18 Epinephrine and norepinephrine are released by nicotine stimulation, and these catecholamines increase myocardial contractility and promote vasoconstriction, which results in increases in BP.”
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“Thirdly, smoking by itself may add to the increased risk profile and target organ damage by inducing insulin resistance (25) and increase in sympathetic nervous activity with release of catecholamines (26).”
BackgroundCigarette Smoking and Its Hazards in Kidney Transplantation
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Effects of cigarette smoking on cardiac autonomic function during dynamic exercise
Mendonça, G. V., Pereira, F. D., & Fernhall, B. (2011) · Journal of Sports Sciences · doi:10.1080/02640414.2011.572991 · Cited by 28
“This agrees with previous findings showing that acute smoking elicits greater sympathetic modulation to the sinus node at rest (Hayano et al., 1990; Grassi et al., 1994; Karakaya et al., 2007; Niedermaier et al., 1993).”
ResultYüksel, R., Yüksel, R. N., Şengezer, T., & Dane, Ş. (2016) · Clinical and investigative medicine · doi:10.25011/cim.v39i6.27519 · Cited by 28
“Endothelial dysfunction, coronary vasoconstriction, platelet aggregation and increased sympathetic activity are trigger mechanisms for these adverse cardiovascular events [6].”
BackgroundAltered pattern of sympathetic activity with the ovarian cycle in female smokers
Park, J., & Middlekauff, H. R. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01197.2008 · Cited by 27
Noborisaka, Y., Ishizaki, M., Yamada, Y., Honda, R., Yokoyama, H., Miyao, M., & Tabata, M. (2012) · Environmental Health and Preventive Medicine · doi:10.1007/s12199-012-0285-7 · Cited by 28
“Orth and Hallan [2] have extensively discussed possible mechanisms underlying the development of CKD in smokers, including heavy metal toxicity due to inhalation of tobacco smoke [20–22], intrarenal vasoconstriction [23–27], and oxidative stress and the inflammatory process [28–30].”
BackgroundMasson, C. L., & Gilbert, D. G. (1999) · Journal of Behavioral Medicine · doi:10.1023/a:1018793729594 · Cited by 27
“This notion is supported by observations that smoking-induced changes in heart rate and blood pressure are associated with an increase in plasma catecholamine concentrations (Grassi et al., 1994; Cryer et al., 1976).”
BackgroundPlasma Catecholamines in Buerger's Disease: Effects of Cigarette Smoking and Surgical Sympathectomy
Roncon‐Albuquerque, R., Serrão, P., Vale-Pereira, R., Lima, J. L. F. C., & Roncon‐Albuquerque, R. (2002) · European Journal of Vascular and Endovascular Surgery · doi:10.1053/ejvs.2002.1721 · Cited by 27
Cigarette smoking lowers blood pressure in adolescents: the Irbid-TRY
Alomari, M. A., & Al‐Sheyab, N. (2016) · Inhalation Toxicology · doi:10.3109/08958378.2016.1145769 · Cited by 26
“…stimulates ‘‘excessive’’ sympathohormonal-excitatory response, including epinephrine, norepinephrine and vasopressin (Al-Kubati et al., 2006; Blank et al., 2011; Cryer et al., 1976; Grassi et al., 1994), which might have mediated an immediate CV changes during smoking (Alomari et al., 2014,2015).”
Background2013 ESH/ESC GUIDELINES FOR THE MANAGEMENT OF ARTERIAL HYPERTENSION
Mancia, G., Fagard, R. H., Narkiewicz, K., Redón, J., Zanchetti, A., Böhm, M., Christiaens, T. C., Cífková, R., Backer, G. D., Dominiczak, A. F., et al. (2014) · Russian Journal of Cardiology · doi:10.15829/1560-4071-2014-1-7-94 · Cited by 26
Self-citationClinical Relevance of the Sympathetic–Vascular Interactions in Health and Disease
Quarti‐Trevano, F., Seravalle, G., & Grassi, G. M. (2021) · Biomedicines · doi:10.3390/biomedicines9081007 · Cited by 27
“, a behavior that is accompanied by a marked increase in blood pressure and heart rate because of the peripheral (and probably central) sympathostimulating effects of nicotine and other smoking products [9].”
BackgroundSelf-citationEffect of smoking on transient evoked otoacoustic emissions and contralateral suppression
Vinay (2009) · Auris Nasus Larynx · doi:10.1016/j.anl.2009.09.013 · Cited by 26
Nicotine increases chemoreflex sensitivity to hypoxia in non-smokers
Argacha, J., Xhaët, O., Gujic, M., Adamopoulos, D. N., Beloka, S., Dreyfuss, C., Degaute, J.-P., & van de Borne, P. (2008) · Journal of Hypertension · doi:10.1097/hjh.0b013e3282f2b93c · Cited by 26
Cigarette Smoking and Blood Pressure in a Worker Population: A Cross-Sectional Study
Fogari, R., Zoppi, A., Lusardi, P., Marasi, G., Villa, G., & Vanasia, A. (1996) · European Journal of Cardiovascular Prevention & Rehabilitation · doi:10.1177/174182679600300108 · Cited by 26
Ba, Z., Xiao, Y., He, M., Liu, D., Wang, H., Liang, H., & Yuan, J. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.810262 · Cited by 25
Middlekauff, H. R., Park, J., Agrawal, H., & GORNBEIN, J. A. (2013) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00502.2013 · Cited by 25
Bianchim, M. S., Sperandio, E. F., Martinhão, G. S., Matheus, A. C., Lauria, V. T., da Silva, R. P., Spadari, R. C., Gagliardi, A. R. T., Arantes, R. L., Romiti, M., et al. (2016) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x20154435 · Cited by 25
“The influence of those factors on pulmonary function has previously been described (16,18,19).”
BackgroundAcute ventilatory and circulatory reactions evoked by nicotine: are they excitatory or depressant?
Fernández, R., Larrain, C. M., & Zapata, P. (2002) · Respiratory Physiology & Neurobiology · doi:10.1016/s1569-9048(02)00185-4 · Cited by 25
Effects of Acute Vaporized Nicotine in Non-Tobacco Users at Rest and during Exercise
Fogt, D. L., Levi, M. A., Rickards, C. A., et al. (2016) · International journal of exercise science · doi:10.70252/foph3992 · Cited by 24
“We recently reported higher resting and orthostatic arterial pressures in young, normotensive non-smokers following acute EC nicotine exposure compared with placebo (10), and suggest that this and our current observations are related to known increases in plasma catecholamines observed with smoking (16).”
ResultSwislocki, A., Tsuzuki, A., Tait, M. G., et al. (1997) · Metabolism · doi:10.1016/s0026-0495(97)90270-5 · Cited by 24
Acute effects of cigarette smoking on the QT interval in healthy smokers
Andrássy, G., Szabó, A., Dunai, A., et al. (2003) · The American Journal of Cardiology · doi:10.1016/s0002-9149(03)00678-7 · Cited by 24
Effect of Smoking Habit on Circulating Adipokines in Diabetic and Non-Diabetic Subjects
Al-Mutairi, S., Mojiminiyi, O. A., Shihab‐Eldeen, A., Sharafi, A. A., & Abdella, N. (2008) · Annals of Nutrition and Metabolism · doi:10.1159/000151487 · Cited by 24
Presynaptic lonotropic Receptors
Dorostkar, M. M., & Boehm, S. (2007) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-74805-2_15 · Cited by 24
Hikosaka, M., Yuasa, F., Yuyama, R., et al. (2002) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-200212000-00008 · Cited by 23
“This technique has been described extensively in previous studies (20,21).”
MethodInfluence of Nicotine from Diverse Delivery Tools on the Autonomic Nervous and Hormonal Systems
Menshov, V. A., Trofimov, A. V., Zagurskaya, A. V., Berdnikova, N. G., Yablonskaya, O. I., & Platonova, A. G. (2022) · Biomedicines · doi:10.3390/biomedicines10010121 · Cited by 25
“Studies in smokers have confirmed that activation of the baroreflex by a pressor response masks the increase in postganglionic sympathetic nerve movement after cigarette smoking [54].”
BackgroundJohansson, J. K., Niiranen, T., Puukka, P. J., & Jula, A. (2010) · Blood Pressure · doi:10.3109/08037051.2010.518675 · Cited by 22
Are current smokers paradoxically protected against atrial fibrillation after cardiac surgery?
Mariscalco, G., & Engström, K. G. (2009) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntn011 · Cited by 21
Limsanon, T., & Kalayasiri, R. (2014) · Behavior Therapy · doi:10.1016/j.beth.2014.10.002 · Cited by 21
Central nicotinic stimulation reduces vascular conductance in the gingiva in anesthetized rats
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Modulation of Transmitter Release Via Presynaptic Ligand-Gated Ion Channels
Schicker, K. W., Dorostkar, M. M., & Boehm, S. (2008) · Current Molecular Pharmacology · doi:10.2174/1874467210801020106 · Cited by 20
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Cardiovascular Sequelae of Tobacco Smoking
Rempher, K. J. (2006) · Critical Care Nursing Clinics of North America · doi:10.1016/j.ccell.2005.10.006 · Cited by 19
“From the pathophysiologic perspective, increases in sympathetic outflow associated with hypertension have been linked with increases in plasma norepinephrine levels [41,42].”
BackgroundPlasma noradrenaline and ageing: effects of smoking habits
Jensen, E. W., Espersen, K., KANSTRUP, L., & Christensen, N. J. (1996) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1996.tb02127.x · Cited by 18
Acute Effects of Cigarette Smoking on Renal Hemodynamics
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The Effect of Smoking on Facial Fat Grafting Surgery
Özalp, B., & Çakmakoğlu, Ç. (2016) · Journal of Craniofacial Surgery · doi:10.1097/scs.0000000000003356 · Cited by 18
Oral Vitamin C Ameliorates Smoking-induced Arterial Wall Stiffness in Healthy Volunteers
Katayama, Y., Shige, H., YAMAMOTO, A., Hirata, F., & Yasuda, H. (2004) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.11.354 · Cited by 17
Miland, Å. O., & Mercer, J. B. (2006) · European Journal of Applied Physiology · doi:10.1007/s00421-006-0261-2 · Cited by 17
“Smoking is associated both with a nicotine-dependent stimulation of the sympathetic system and an inactivation of vagal cardiovascular control (Grassi et al. 1994; Groppelli et al. 1992), and smoking also”
Background
Metadata
- Authors
- Grassi, G., Seravalle, G., Calhoun, D. A., Bolla, G. B., Giannattasio, C., Marabini, M., Del Bo, A., & Mancia, G.
- Affiliations
- Azienda Ospedaliera San Gerardo (IT)
- Cattedra Medicina Interna, Ospedale S. Gerardo dei Tintori, Monza, Italy.
- Venue
- Circulation
- Published
- 1994-07
- Volume
- 90
- Issue
- 1
- Pages
- 248-253
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- OpenAlex
- W2034576097
- Cited by
- 394
- References
- 0
- Citations by year
- 2026: 11 · 2025: 7 · 2024: 11 · 2023: 7 · 2022: 9 · 2021: 15 · 2020: 16 · 2019: 12 · 2018: 12 · 2017: 10 · 2016: 14 · 2015: 12 · 2014: 13 · 2013: 26 · 2012: 16
- FWCI
- 4.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion)
- Funders
- National Institutes of Health (5k11hl002568-05, 5k08hl003220-02)
- National Heart, Lung, and Blood Institute (HL 03220, HL02568)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Smoking Behavior and Cessation
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Blood Pressure and Hypertension Studies
- Keywords
- cigarette smoking, sympathetic nervous system, baroreflex, baroreflex sensitivity, plasma catecholamines, norepinephrine, epinephrine, muscle sympathetic nerve activity, blood pressure, heart rate, vascular resistance, nicotine, hemodynamic response, reflex mechanisms, phenylephrine infusion, normotensive subjects
- MeSH terms
- Adult, Blood Pressure, Female, Heart Rate, Humans, Male, Middle Aged, Muscles, Norepinephrine, Phenylephrine, Smoking, Sympathetic Nervous System
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