Effects of passive smoking on blood pressure and aortic pressure waveform in healthy young adults influence of gender
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1 DOI: /j x British Journal of Clinical Pharmacology Effects of passive smoking on blood pressure and aortic pressure waveform in healthy young adults influence of gender Azra Mahmud & John Feely Department of Pharmacology and Therapeutics, Trinity College Dublin and Hypertension Clinic, St James s Hospital, Dublin 8, Ireland Correspondence Professor John Feely, Department of Pharmacology & Therapeutics, Trinity Centre for Health Sciences, St James s Hospital, Dublin 8, Ireland. Tel: Fax: jfeely@mail.tcd.i.e Keywords arterial stiffness, augmentation index, blood pressure, gender, passive smoking Received 21 October 2002 Accepted 24 February 2003 Ai Passive smoking impairs the elasticity of the aorta in patients with coronary heart disease. We therefore studied the effect of passive smoking on wave reflection in the aorta, a marker of arterial stiffness, in healthy subjects. Method We examined the effects of acute exposure to passive smoking on blood pressure and the aortic pressure waveform in healthy young men (n = 10) and women (n = 11), aged 26 ± 5 years (mean ± SEM) compared with 12 healthy controls, aged 24 ± 2 years (six female) who were exposed to room air. The aortic pressure waveform was derived with radial applanation tonometry (SphygmoCor, AtCor Medical, version 6.2) and the augmentation index, a measure of arterial wave reflection in the aorta, calculated. Blood pressure (Omron Model HEM-5 CP, Omron Corporation, Tokyo, Japan) and augmentation index were measured at baseline, 15, 30 and min after exposure to environmental tobacco smoke (carbon monoxide p.p.m. for min) or room air. Results Passive smoking was associated with an increase in brachial (124 ± ± 3, P < 0.01) and aortic systolic blood pressure ( ± ± 4, P < 0.01) at min in the male subjects only. The augmentation index increased from -1.7 ± 5 to 14 ± 5 at min (P < 0.001) only in the male subjects. The transit time of the pulse did not change significantly. The change in augmentation index was independent of the increase in blood pressure. Brachial and aortic diastolic blood pressure and heart rate did not change significantly in either male or female subjects. No haemodynamic changes were observed in the control group. Conclusions Acute exposure to passive smoking has a deleterious effect on the arterial pressure waveform in healthy young males but not in females, suggesting a possible protection of female gender from functional changes in arteries Blackwell Publishing Ltd Br J Clin Pharmacol 57:
2 A. Mahmud & J. Feely Introduction Passive smoking is associated with the development of atherosclerosis, coronary artery disease and stroke [1, 2]. Among possible mechanis, the effect of passive smoking on the mechanical properties of the arterial wall may play an important role in generating cardiovascular dysfunction. Active smoking alters endothelial function [3] and induces coronary vasoconstriction [4]. We have recently shown that young healthy chronic smokers have much stiffer arteries than age-matched nonsmokers and acutely cigarette smoking stiffens arteries [5]. Long-term passive smoking has been shown to impair endothelium-dependent vasodilatation in healthy adults [6], which is potentially reversible [7]. A recent study has shown that acute exposure to passive smoking generates endothelial dysfunction in the coronary arteries in both smokers and nonsmokers [8]. An invasive study in men with coronary artery disease has shown that acute exposure to passive smoking impairs elastic properties of the aorta [9]. The aorta and large arteries serve a major function in the cardiovascular system as a conduit and buffering organ. Increased arterial stiffness is associated with a number of risk factors, including age, smoking, hypertension, diabetes, hypercholesterolaemia and atherosclerosis [10] and is of prognostic significance in hypertension and end-stage renal disease [11 13]. Large arteries buffer the pressure changes resulting from intermittent ventricular ejection of blood into the aorta. By absorbing a proportion of the energy in systole and releasing it in diastole, they not only maintain coronary blood flow but also avoid an increase in left ventricular afterload while smoothing out blood flow to the periphery. Pressure waves are reflected back from the periphery and summate with the forward-going wave to produce the characteristic aortic pressure waveform. When the ventricular-vascular coupling is optimal, the reflected waves fall in the diastolic portion of the arterial pressure wave and so do not influence aortic systolic pressure but enhance coronary blood flow. However, with vascular stiffening, pulse wave velocity and the amplitude of the reflected waves both increase, such that the reflected wave arrives earlier and augments central systolic pressures. Thus early wave reflection elevates systolic and pulse pressure and impedes coronary perfusion [14]. The technique of pulse wave analysis can be used to assess aortic blood pressure (BP) noninvasively [14] and a high augmentation index (AIx), a measure of arterial wave reflection, is closely related to aortic stiffness [14]. As we have recently shown that acute cigarette smoking increases arterial wave reflection [5] we hypothesized that acute exposure to passive smoking may also lead to detrimental effects on the aortic pressure waveform in healthy adults. Methods Study population We studied 21 healthy subjects (10 male, 11 female) aged 26 ± 1.6 years, height and weight 1.7 ± 1.7 cm and 66 ± 1.9 kg (mean ± SEM), respectively, following exposure to passive smoking. We also studied 12 healthy subjects (six females) as controls, aged 24 ± 2 years, height and weight 172 ± 1 cm and 68 ± 2 kg (mean ± SEM), respectively. All the participants were normotensive (blood pressure </ ) and were nonsmokers, exposed to environmental tobacco smoke only very occasionally in their daily lives. None of the subjects was taking any medications. The study had institutional ethics committee approval. Study protocol The subjects were studied fasting, having abstained from alcohol or caffeine-containing beverages in the 12 h prior to the study. All haemodynamic measurements were made in the supine position with a 15-min rest before baseline. A mean of three readings was taken. After stable baseline measurements, a series of 15 cigarettes (nicotine content: each 1.2 mg) were lit at a sufficient rate to maintain a carbon monoxide concentration between 25 and 30 p.p.m. (confirmed by Multiwarn II, Draeger Instruments, UK) in an unventilated room over 1 h. The subjects acting as controls were studied in an identical manner breathing room air. Blood pressure measurements The haemodynamic measurements were performed in a quiet room at C after resting for 15 min. Brachial BP and heart rate were measured in the left arm with an automated digital oscillometric BP monitor (Omron Model HEM- 5 CP, Omron Corporation, Tokyo, Japan). Brachial mean arterial pressure (MAP) was calculated by integration of the pressure waveform using the SphygmoCor version 6.2 software (AtCor Medical, Sydney, Australia). A mean of three readings was taken. Derivation of the aortic pressure waveform Immediately after taking the final blood pressure reading, the same arm was used for applanation tonometry. We have found that using the contralateral arm or performing tonometry before blood pressure measurements 38 57:1 Br J Clin Pharmacol
3 Vascular effects of passive smoking does not alter the readings. A high-fidelity micromanometer (SPC-301, Millar Instruments, Texas, USA) was used to flatten the radial artery and the peripheral radial pulse continuously recorded. The data were fed directly into a computer, 20 sequential radial waves were averaged by the computer software and an averaged aortic pressure waveform was generated using the generalized transfer function (SphygmoCor, Atecor Medical, version 6.2) as previously described [5]. The aortic pressure waveform was used to generate the AIx, ascending aortic pressures and heart rate. The AIx was calculated from the aortic pressure waveform as height of the late systolic peak divided by pulse pressure. The validity of these derived values has been confirmed by simultaneous direct aortic measurements and is highly reproducible in both healthy and diseased populations [15 19]. The transit time (Tr) of the reflected wave was measured from the foot of the pressure wave to the inflection point of the wave as described previously [20, 21]. Left ventricular ejection duration (LVED) was measured from the foot of the aortic pressure wave to the diastolic incisura. Statistical analysis Descriptive analyses are presented in the form of mean ± SEM for normally distributed data. The time dependent patterns of haemodynamic changes were studied by analysis of variance of repeated measures testing for a gender, time and gender by time interaction effect. Furthermore, to see if changes in AIx were dependent on changes in BP three-way analysis of covariance was performed, correcting changes in AIx for the change in MAP over time. A significance level of a = 0.05 is assumed throughout. The statistical analysis was performed with JMP software, version 3.0 (SAS Institute, Cary, NC). Results There was no difference in the baseline haemodynamic parameters of the passive smokers and the control group (Table 1). The brachial and aortic systolic BP were significantly higher (P < 0.05) in the male passive smokers compared with females. The females had a significantly shorter Tr (P < 0.05) than males. There was no significant difference in AIx and LVED between the male and female subjects at baseline (Table 1). There was no change seen in blood pressure, heart rate or AIx in the control group studied over min breathing room air. Effects of passive smoke exposure on blood pressure and heart rate There was a clear difference in the haemodynamic response of male and female subjects following passive smoking (Table 2). The brachial systolic BP increased significantly over time in the male subjects only, from ± 3 at baseline to 137 ± 3.4 at the end of min (P < 0.001) but not in the females (P > 0.2). The aortic systolic BP also increased over time (P < 0.001) in the male subjects only, from ± 3.4 at baseline to 123 ± 4.3. There was no significant change in the brachial or aortic diastolic BP pressure, heart rate and LVED in both males and females. Changes in the aortic pressure waveform A characteristic abnormality was observed in the radial and aortic pressure wavefor during passive smoking in males, with the reflected waves moving from diastole to the systolic part of the blood pressure curve and increased in amplitude (Figure 1). This was associated with a significant rise in the AIx, from -1.7 ± 5.2 at baseline to 14 ± 4.8 at the end of min in males (P < 0.001) but not in the female subjects though a transient fall was seen at 15 min in females (Figure 2). The increase in AIx in the male subjects occurred at 15 min, Table 1 Baseline haemodynamic parameters in males (n = 10) and females (n = 11) exposed to passive smoking and control subjects (n = 12). Data presented as mean ± SEM (males compared with females *P < 0.05). Passive smoking group Males Females Controls Brachial SBP () ± 3* 114 ± ± 3 Brachial DBP () 79 ± ± 3 74 ± 4 Aortic SBP () ± 3.4*.4 ± ± 4 Aortic DBP () ± ± ± 1 Heart rate (beats min -1 ) 68 ± ± ± 1.4 Augmentation index (%) -1.7 ± ± ± 1.3 DTr () 151 ± 7* 133 ± ± 5 LVED () 301 ± ± ± 7 Br J Clin Pharmacol 57:1 39
4 A. Mahmud & J. Feely Table 2 The effect of passive smoking on brachial and aortic blood pressure and heart rate at baseline, 15, 30 and min after exposure. An effect was seen on systolic BP and DTr in male subjects only. Mean ± SEM, (*P < 0.05 from baseline) Time (min) Brachial BP () Aortic blood pressure () Systolic Diastolic Systolic Diastolic DTr () Male Female Male Female Male Female Male Female Male Female ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± 3.4* ± ± ± ± 3.8* 96.1 ± ± 4 76 ± ± ± ± 3.4* ± ± ± ± 4.3* 98.5 ± ± ± ± ± 3.5 RADIAL PULSE WAVEFORM RADIAL PULSE WAVEFORM AORTIC PULSE WAVEFORM AORTIC PULSE WAVEFORM Figure 1 Radial and aortic pressure wavefor at baseline (top panel) and at min following exposure to passive smoking (bottom panel). 1 and 2 represent the early and late systolic pressure peaks. There is an increase in amplitude of the reflected wave (Ø) in the aortic pressure wave form preceding the rise in both brachial and aortic systolic BP, which occurred from 30 min onwards. The increase in AIx was still statistically significant (P < 0.05) when corrected for the increase in MAP. The Tr decreased in the males following exposure to passive smoking but it was not statistically significant. Discussion Active cigarette smoking is accepted as a cause of atherosclerotic heart disease and recently exposure to passive smoking has also been identified as a cardiovascular hazard, including stroke [1, 2] with major public health implications. The acute response of BP and heart rate to environmental tobacco smoke exposure is uncertain with both an increase in BP and heart rate following passive smoking [7, 22] or no effects [23] reported. The systolic BP increased significantly in the present study after 30 min of exposure to passive smoking in the male subjects only. The diastolic BP showed a trend towards an increase in males but there was no increment in heart rate. Arterial stiffness increases in both elastic and muscular arteries after acute cigarette smoking [5, 24 26] :1 Br J Clin Pharmacol
5 Vascular effects of passive smoking Augmentation index (%) Figure 2 Arterial wave reflection, measured as augmentation index, increased significantly over time in male subjects only during exposure to passive smoking over min. Data presented as mean ± SEM. Male ( ); and female ( ) * Recently, Stefanadis et al. have shown by invasive methods, that acute exposure to passive smoking increases both systolic and diastolic blood pressure and impairs elastic properties of the aorta in middle-aged and older males with coronary artery disease [9]. The important finding in our study is that this deleterious vascular effect of passive smoking on the aortic pressure waveform is also seen in healthy young subjects and within 15 min of exposure. The AIx, a manifestation of early wave reflection, increased at 15 min and was still elevated at the end of min following exposure to environmental tobacco smoke in males. The arterial pressure waveform in both the radial artery and the aorta showed abnormalities in the male subjects (Figure 1). The increase in AIx seen in response to passive smoking in the male subjects can be due to a number of mechanis including enhanced arterial wave reflection as a consequence of increased vascular tone, an increase in pulse wave velocity and changes in left ventricular ejection or a combination of these factors. There was no change in heart rate or left ventricular ejection duration. While the pulse wave velocity was not formally measured the pulse transit time of the reflected wave which has been used as a surrogate for pulse wave velocity [20, 21] did not change significantly although there was a trend for a decrease. The shorter Tr in women at baseline is largely explained by their shorter stature with less distance for the reflected wave to travel. We therefore believe that the increased arterial wave reflection in the aorta secondary to increased peripheral vascular tone was primarily responsible for the increase in AIx. * Time (min) * It was not possible to determine the exact mechanism whereby passive smoking produced this effect and to what extent it is related to smoke-induced changes in BP but our results suggest that the increase in AIx is independent of the increase in BP. The increased vascular tone could be due to sympathetic nervous system activation and passive smoking increases sympathetic drive [27] which stiffens both elastic and muscular arteries [28]. The enhanced wave reflection in our study could also be due to endothelial dysfunction as it has been shown that passive smoking is associated with a dose-related impairment of endothelium-dependent dilatation in healthy subjects [6, 8] and endothelial dysfunction may be related to arterial stiffness [29]. However, short-term exposure to passive smoking has not been shown to affect either endothelium-dependent or independent vasodilatation in healthy adults [23]. Other possible mechanis for the acute detrimental effects on the vascular wall following exposure to tobacco smoke include platelet activation [30], impaired endothelial release of prostacyclin [31] and increased vasopressin release [32]. The observation that changes in wave reflection were seen at 15 min prior to the increase in BP suggests that more than one mechanism may be involved. The female subjects in the study did not show any harmful effects on the arterial pressure waveform when exposed to tobacco smoke. We noted an acute fall in the AIx in female subjects at 15 min, which may in part be explained by a small increase in heart rate, which tends to decrease the AIx [33]. Also there was a tendency for BP, particularly aortic to fall in the female subjects while it continued to rise steadily in the male subjects. All the females in the study were young healthy premenopausal women, suggesting that the sensitivity of the female arterial wall to smoking is attenuated at least in the younger age group. Brachial flow-mediated dilatation is not decreased in female current smokers compared with former smokers whereas it was decreased in current male smokers compared with ex-smokers [6]. Furthermore, smoking was associated with increased intimamedia thickness in male subjects only [34]. The mechanism may involve circulating oestrogens, as premenopausal females are protected from coronary heart disease [35] and hormone-replacement therapy has a favourable effect on aortic compliance and the aortic pressure waveform in postmenopausal women [36, 37]. We would like to enter certain caveats. The derivation of AIx depends upon the validity of the transfer function and there is some debate in the literature as to how accurate is the application of a generalized transfer function in subjects of all ages both in health and in illness. Br J Clin Pharmacol 57:1 41
6 A. Mahmud & J. Feely However, a recent study by Soderstrom et al. [19] has shown that directly measured and synthesized aortic pressure wavefor were very similar in patients with coronary artery disease and furthermore the changes in the measured and synthesized aortic pressure wavefor secondary to nitroglycerin and midazolam are very similar. However, more studies are needed to validate further the derivation of AIx especially in young subjects with normal and compliant arteries. Also, we have presented our blood pressure data in the form of systolic and diastolic blood pressures and not pulse pressure. In populations under the age of 40 years, there is an inverse relationship between pulse pressure and cardiovascular risk as shown in the Framingham study [38]. Therefore, we do not consider this is an appropriate surrogate of stiffness in a young population. Indeed, we have also shown recently that some young males with spurious systolic hypertension of youth despite having very elastic arteries, have a wide pulse pressure which is largely attributable to high pulse pressure amplification [39]. The levels of side-stream smoke used in our study mimic the intensity of acute exposure in real life situations [40, 41], such as a smoky bar and are within the guidelines for maximum allowable exposure to passive smoking [42]. The effect of this level of exposure on the vasculature is considerable, producing abnormalities of aortic pressure waveform of a magnitude that we would commonly see in mild hypertension [43]. Such a level of exposure has recently been shown to reduce the coronary flow velocity reserve in healthy young men [8] and also impairs the elastic properties of the aorta in patients with coronary heart disease [9]. While burning cigarettes as in our study produced side-stream smoke, as opposed to exhaled smoke (main-stream), it has also been shown that actively smoking one filtered cigarette also causes an acute deterioration of aortic elastic properties [5, 26]. We now need further information on the effects of lesser degrees of exposure to passive smoking, especially in the high-risk populations, such as patients with hypertension, diabetes and coronary heart disease. This work was in part supported by the Royal City of Dublin Hospital Research Fund. References 1 Jiang HE, Vupputuri S, Allen K, Prerost MR, Hughes J, Whelton PK. Passive smoking and the risk of coronary heart disease a meta analysis of epidemiological studies. N Engl J Med 1999; 340: Bonita R, Duncan J, Teuelsen T, Jackson RT, Beaglehole R. Passive smoking as well as active smoking increases the risk of acute stroke. Tobacco Control 1999; 8: Calermajer DS, Sorensen KE, Georgakopoulos D, et al. 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