A systematic literature review was conducted using PubMed, Embase and the Cochrane Library to determine the effect of acute, chronic and passive smoking on arterial stiffness and to determine whether these effects are reversible after smoking cessation. A total of 39 relevant studies were identified and included. Acute smoking was found to cause an acute increase in arterial stiffness. Similarly, passive smoking increased arterial stiffness acutely and chronically. The majority of studies identified chronic smoking as a risk factor for increasing arterial stiffness. However, some studies found no statistical difference in arterial stiffness between nonsmokers and long-term smokers, although chronic smoking seems to sensitize the arterial response to acute smoking. In addition, whether arterial stiffness is reversed after smoking cessation and the timeline in which this may occur could not be determined from the identified literature. The effect of smoking discontinuation on arterial stiffness remains to be established by prospective smoking cessation trials.
Cigarette smoking has long been established as a cardiovascular risk factor and is the major preventable cause of death and disability in developed and developing countries.1, 2 Smoking accounts for ∼1 200 000 deaths each year in Europe, 440 000 in the United States and 50 000 in Canada.1, 2, 3 Smoking can cause cardiovascular damage by inducing endothelial dysfunction and harmful hemodynamic effects, such as increased arterial stiffness.4, 5, 6 Furthermore, a number of factors and conditions, such as alcohol consumption, dyslipidemia, hypertension, renal dysfunction, obesity and chronic obstructive pulmonary disease cause changes in arterial stiffness.7, 8, 9, 10, 11, 12, 13, 14 These effects may interact with the effects of smoking to alter arterial stiffness and cardiovascular risk profiles.
The measurement of vessel hemodynamics is gaining popularity as a means to assess arterial stiffness and endothelial function. Accordingly, various noninvasive methods have been developed to measure arterial stiffness, including applanation tonometry, echotracking, Doppler and ultrasound.15 These techniques could be useful in clinical practice, particularly applanation tonometry, as numerous studies have shown that increased arterial stiffness as measured by aortic pulse wave velocity (PWV) and augmentation index (AIx) is directly and independently associated with increased risk of cardiovascular complications and events.16, 17, 18, 19, 20, 21, 22 Although aortic PWV (typically measured by carotid-femoral PWV (cfPWV)) has the most evidence to support its predictive value for cardiovascular events, it is important to understand the differences between PWV measured in various vascular beds; smoking may affect particular areas of the vascular system in different ways. cfPWV reflects the stiffness of the central elastic arteries, crPWV (carotid-radial PWV) and brPWV (brachial-radial PWV) reflect the stiffness of peripheral muscular arteries, and brachial-ankle PWV (baPWV) is an intermediate measurement, providing information about the stiffness of both peripheral muscular and central elastic arteries.15, 16
The purpose of this systematic review was to assess the effect of acute, chronic and passive smoking on arterial stiffness, as well as the effect of smoking cessation on arterial stiffness.
Data sources and study selection
Studies were identified through PubMed, Embase and the Cochrane Library using the keywords shown in Figure 1. Relevant articles were extracted using search terms, reference lists and the ‘related article’ links of articles selected for review. We included all relevant clinical studies that enrolled chronic smokers and nonsmokers in whom arterial stiffness was measured. The search for articles was limited to those published between 1985 and November 2009, and written in English. Two independent researchers (RJD and AH) conducted the search.
A total of 39 studies were identified, confirmed by all authors and included in this review. Figure 1 illustrates the search and study selection procedure. Tables 1,2,3,4 summarize the findings of the included studies, and Supplementary Tables 1–4 summarize the patient characteristics of the included studies.
The acute effects of cigarette smoking on arterial stiffness have been explored previously (Table 1). A number of studies have shown that arterial stiffness increases acutely after cigarette or cigar smoking as measured by AIx, cfPWV, brPWV or crPWV.23, 24, 25, 26 Another study between chronic and nonsmokers reported that at baseline, the baPWV was not significantly different but was significantly higher in chronic smokers 5 min after cigarette smoking and remained higher for 30 min (P<0.05); in both groups, baPWV was significantly higher at 5 min when compared with baseline (both P<0.001) and returned to baseline at 45 min.27
Rhee et al.28 reported a significant smoking-induced acute increase in heart-femoral PWV (P<0.05). However, after adjustment for total cholesterol, time-dependent heart rate and brachial mean arterial pressure, this association lost statistical significance.
The acute effects of smoking were also evaluated on aortic, carotid, radial and brachial distensibility and compliance; in all studies, distensibility and compliance decreased in all arterial beds studied.29, 30, 31, 32, 33, 34 Swampillai et al.35 reported a significant smoking-induced increase in stiffness index (SI) 15 min after smoking (P<0.05), but did not observe changes in wave speed in the carotid artery.
Several studies reported the relationship between PWV and smoking (Table 2). In one study, brPWV was significantly increased in smokers;36 another study reported higher PWV in smokers, but did not report the arterial segment that was measured.37 Similarly, increases in aortic stiffness were also noted in smokers in other studies.38, 39 In fact, cigarette smoking was found to be a significant predictor of increased aortic PWV in White and Black individuals (R2=0.13 and R2=0.14, respectively; P<0.05).39 In contrast, Yufu et al.40 found no significant differences between smokers and nonsmokers when evaluating baPWV. In addition, three different groups found no significant correlation between smoking status and increased cfPWV.41, 42, 43 However, AIx was increased in smokers (17.25%) compared with nonsmokers (11.75%; P=0.004) in one of the same subject populations.42 A number of other studies found AIx to be increased in chronic smokers compared with nonsmokers.24, 41, 44, 45 Furthermore, Tomiyama et al.46 showed that AIx was independently correlated with smoking status in men and women.
Some of the identified studies evaluated arterial stiffness using ultrasonographic methods: SI, distensibility and compliance. Two studies reported that smokers had significant increases in the SI when compared with nonsmokers.47, 48 However, another study only reported significant increases in SI in female smokers (P=0.041).49 Aortic compliance50 and aortic distensibility51 were significantly decreased in smokers compared with nonsmokers. In a study of smoking adolescents, the normalized pressure strain in smokers was higher than in nonsmokers (P=0.001).52 McVeigh et al.53 found that the damping of diastolic oscillation was significantly increased in smokers, and that the derived oscillatory compliance estimate was reduced compared with nonsmokers. Another study also found stiffer arteries in chronic smokers; however, this was limited to the popliteal artery.54 Nevertheless, one study found no difference in carotid and brachial artery distensibility between nonsmokers and chronic smokers.32
Three different studies found that exposure to environmental tobacco smoke (ETS) for 5–60 min leads to increased arterial stiffness (Table 3).34, 55, 56 However, in one study, this change was noted only in male subjects.56 No change was observed after exposure to nontobacco smoke in any of the studies.34, 55, 56 Interestingly, administration of sublingual nicotine was associated with increased AIx (P=0.001).55 Another study reported a significant correlation between carotid arterial SI and ETS exposure. In older individuals, or in those with increased intima–media thickness, the adjusted SI was increased with increasing number of ETS sources (P=0.09 and P=0.05, respectively). In individuals with a higher body mass index, or in those with increased intima–media thickness, the adjusted SI was increased within hours of exposure to ETS (both P=0.04).57
The effect of smoking cessation in reversing increased arterial stiffness is not well established (Table 4). Oren et al.58 and Polonia et al.59 observed a decrease in AIx after 6 months of smoking cessation; continuing smokers showed no such change.58, 59 Rehill et al.42 reported similar results after only 4 weeks of smoking cessation. In contrast, another study reported no significant change in arterial stiffness between persistent smokers and in individuals who stopped smoking for 2 years as assessed by the distensibility of the carotid and femoral arteries.60 Furthermore, Polonia et al.59 found that no change occurred in cfPWV after 6 months of smoking cessation.
In this systematic review, we presented results obtained from 39 studies evaluating the effect of smoking on arterial stiffness. These studies show that acute, chronic and passive smoking has a detrimental effect on arterial stiffness, and that smoking cessation may improve arterial stiffness. However, further work is required to definitively determine whether arterial stiffness is improved over time after smoking cessation and the timeline in which this occurs.
The effect of acute smoking is clear cut, causing an acute increase in arterial stiffness in both chronic smokers and nonsmokers. All studies, except one, found that acute smoking causes a significant increase in arterial stiffness in chronic smokers. The study that found no effect was small (30 patients) which actually showed, before adjustment, an increase in heart-femoral PWV after acute smoking.28 Interestingly, chronic smokers had a greater increase in arterial stiffness after acute smoking than did nonsmokers.24, 27 These results are in line with those of previous studies measuring acute smoke-induced endothelial dysfunction measured by flow-mediated dilatation (FMD); endothelial dysfunction was more prolonged in smokers than in nonsmokers.61
The effect of chronic smoking on endothelial dysfunction is also detrimental; studies comparing the FMD of habitual smokers and nonsmokers found smoking to be associated with greater endothelial dysfunction.6, 62 However, the effect of chronic smoking on arterial stiffness is slightly more controversial. Most studies found that chronic smoking increases arterial stiffness as measured by PWV, AIx, SI, compliance and distensibility.24, 36, 37, 38, 39, 47, 48, 49, 50, 51, 52, 53, 63 However, a few other studies did not consistently find this effect.32, 40, 41, 42 For example, Filipovsky et al.41 and Rehill et al.42 found that AIx was significantly higher in smokers than in nonsmokers, while differences in PWV did not reach significance. Kool et al.32 also did not find significant differences between smokers and nonsmokers when measuring compliance and distensibility; however, they only included 14 nonsmokers. Yufu et al. also failed to show a significant difference in baPWV between smokers and nonsmokers; however, they included young, healthy smokers with small cumulative tobacco consumption. Furthermore, in this study, the FMD was strongly correlated with the baPWV (P<0.005).40 It is also noteworthy that PWV was not measured in the same sites in the vascular bed between studies.
Passive smoking clearly causes increased arterial stiffness. Three studies showed that acute exposure to ETS leads to increased stiffness,34, 55, 56 whereas one study found an association between the increased number of ETS sources and the increased time of exposure with a higher SI.57 Furthermore, sublingual nicotine administration was shown to increase AIx, indicating that the effect of smoking on arterial stiffness may act through nicotine.55 Second-hand smoke also causes endothelial dysfunction;5, 64 a study comparing the endothelial function of nonsmokers who were currently or previously exposed to second-hand smoke found that being exposed for ⩽1 h per day for ⩽2 years can cause endothelial dysfunction lasting as long as 2 years after cessation of exposure.64
It has been suggested that smoking-induced damage to the endothelium may be somewhat reversible; former active and passive smokers have better endothelial function than do current active or passive smokers.65, 66 The beneficial effects of smoking cessation on the risk for cardiovascular disease67, 68, 69 and for endothelial dysfunction65, 66 have been established. However, it remains controversial whether arterial stiffness improves after smoking cessation; some studies show rapid improvement in AIx after smoking cessation,42, 58, 59 whereas cfPWV did not improve after 6 months,59 and another study showed no improvement in distensibility after 2 years.59, 60 A cross-sectional study of middle-aged hypertensive patients found that AIx, cfPWV and Tr (transit time) returned to baseline levels only after 10 years of smoking cessation.70 These inconclusive results emphasize the need for long-term longitudinal studies to clarify the controversy on the effect of smoking cessation on arterial stiffness.
Active and passive smoking alters lipid metabolism acutely and chronically (Figure 2).71, 72 Cigarette smoke alters catecholamine release and lipoprotein lipase activity; consequently, free fatty acid release is altered and triglycerides cannot be cleared from the blood.72 This causes an increase in triglycerides and low-density lipoprotein, and a decrease in high-density lipoprotein in the plasma of smokers.71, 72 Changes in lipid metabolism contribute to structural changes of the arterial wall including intima–media thickening and atherogenesis73, 74 and may lead to an increase in arterial stiffness. Furthermore, treatment of the underlying hypercholesterolemia using statins has been shown to decrease arterial stiffness.75, 76
Chronic smoking damages the kidney by causing a loss of filtration rate and contributes to kidney failure.77, 78 In fact, smoking is also correlated with albuminuria in healthy individuals.78 As even mild renal insufficiency leads to collagen accumulation in elastic arteries as well as calcification,79 these smoking-induced alterations in kidney function increase arterial stiffness by altering the structure of the arteries.
Smoking increases insulin release and causes insulin resistance,72, 80 both of which have been shown to increase arterial stiffness.81, 82, 83 Gordin et al.81 showed that mean daily glucose correlated with aortic PWV in diabetic subjects. Similar results have been found in various patient groups.82, 83 In fact, aortic PWV has been shown to increase even in early insulin-resistance states.83 Smoking is also frequently associated with decreased physical activity and poor diet, further increasing adiposity and insulin-resistant states.80
Acute and chronic smoking has been shown to induce oxidative stress, altering vascular tone and increasing arterial stiffness.4, 84 Smoking increases the production of reactive oxygen species, which decreases the activity of nitric oxide synthase (NOS), inhibiting nitric oxide (NO) production by the endothelium.85, 86 Platelet-derived NO production also decreases contributing to a hypercoagulable state.87 Moreover, active and passive smoking decrease total body antioxidant levels,71 which increases endothelial dysfunction and arterial stiffness.85, 88, 89 In fact, total antioxidant capacity is inversely associated with AIx (r=−0.24, P<0.02).82 Treatment of smokers with antioxidants or L-arginine, a NOS substrate, improves FMD and arterial stiffness.85, 90
Smoking has also been shown to cause an inflammatory state by simultaneously increasing proinflammatory and decreasing anti-inflammatory cytokines.91 Various studies have shown strong associations between inflammatory markers and arterial stiffness.92, 93, 94 For example, Vlachopoulos et al. used a Salmonella typhi vaccine to induce inflammation in healthy subjects.95 They found a vaccine-induced increase in cfPWV and a decrease in AIx, which were associated with increases in C-reactive protein and interleukin-6 (biochemical markers of inflammation). Inflammation also causes vascular calcification and release of matrix metalloproteinases, which contribute to vascular remodeling.96
Smoking increases blood pressure and the risk for hypertension.97, 98, 99, 100 Studies have shown that in subjects with hypertension, arterial stiffness is increased compared with normotensive subjects of the same age.101, 102, 103 This increased stiffness leads to elevated systolic pressure and a widened pulse pressure which, in turn, leads to further tension on the arterial wall generating a positive feedback effect.104, 105 The wall tension induces mechanical vessel wall damage, vascular hypertrophy, increased collagen and calcium deposition, smooth muscle cell restructuring and extracellular matrix deposition, which leads to increases in arterial stiffness and end-organ damage, such as left ventricular hypertrophy.105, 106, 107, 108, 109, 110 Treatment of hypertension may help to decrease arterial stiffness; a number of studies have found that antihypertensive therapy can lead to decreased arterial stiffness in addition to blood pressure lowering.111, 112, 113, 114, 115 However, smoking has been found to blunt the arterial stiffness-lowering effect of antihypertensive therapy. Matsui et al.113 treated hypertensive smokers and nonsmokers with amlodipine for 6 months and noted that reduction in baPWV in smokers only reached the level of nonsmokers after 6 months of treatment. Therefore, it seems that smoking and hypertension exert synergistic effects on arterial stiffness, potentially through oxidative stress and the production of reactive oxygen species leading to degradation of NO, and by changes in production of endothelin-1 and prostacyclins.14, 106, 116, 117, 118, 119, 120, 121
As discussed above, numerous previous studies have shown that smoking causes significant endothelial dysfunction as assessed by FMD.5, 6, 61, 62, 64 However, it is important to note that FMD has been previously shown to be significantly associated with arterial stiffness under a number of conditions and disease states.122, 123, 124, 125, 126 Wright et al.127 noted that this association was weak and suggested that measurements of arterial stiffness should not replace FMD. However, they used neither AIx nor cfPWV (the ‘gold standard’) as arterial stiffness measurements in their study. Furthermore, Yufu et al.40 found FMD to be strongly correlated with baPWV in healthy smokers (P<0.005). In addition, Siasos et al.90, 128 showed that smokers under L-arginine treatment have an increase in FMD concurrently with decreases in both AIx and cfPWV.
A number of blood markers carry potential to monitor the progression of arterial stiffness in smokers. Smokers have significantly higher plasma levels of homocysteine, fibrinogen, C-reactive protein, interleukin-6, triglycerides, low-density lipoprotein, as well as decreased high-density lipoprotein and apolipoprotein A1 levels.129, 130, 131 Many of these blood markers and others (such as lycopene, uric acid, adiponectin) have been related to increased arterial stiffness and may also have value in monitoring arterial stiffness in smokers and former smokers.39, 94, 95, 132, 133, 134, 135, 136, 137 However, it has been suggested that the use of multiple blood markers is of little prognostic value,96, 138 and that even the use of single markers such as C-reactive protein or homocysteine did not improve prediction of outcome using the Framingham risk score.138 Perhaps simply measuring cfPWV and AIx may prove the simplest and most effective method to assess and monitor vascular health in smokers.
This review is limited by the comparability of the studies included. Protocols and methods were not standardized; the time of day the study took place, whether the subjects fasted or refrained from alcohol and caffeine before the study were different between protocols, and some did not report this information. Furthermore, the age groups of subjects, duration and intensity of smoking, body mass index, renal function, menopausal status, lipid profile, medication use, including statin use, were not uniform between studies or subject groups. These factors were also often not reported or corrected for; clearly, future studies investigating the effect of smoking on arterial stiffness should recruit homogeneous populations. The majority of the identified studies are cross-sectional; however, population-based longitudinal studies would be better suited to study the effect of smoking on arterial stiffness and to better track the progression of improvement in arterial stiffness after smoking cessation. Perhaps the most pertinent limitation of the included studies is the different methods used to obtain information about arterial stiffness. cfPWV is the ‘gold standard’ for measurement of arterial stiffness, and cfPWV and AIx have the greatest amount of evidence to support their predictive value for cardiovascular events.16, 17, 18, 19, 20, 21, 22 Therefore, other parameters of arterial stiffness, such as local distensibility or compliance, may not be as valuable to assess the vascular effects of smoking and are not useful clinical parameters. These should be used sparingly compared with cfPWV and AIx. Owing to these limitations of the included studies, a meta-analysis aiming to quantify the overall magnitude of the effect of smoking on arterial stiffness could not be conducted. However, the results of the included studies are comparable and point to smoking having a detrimental effect on arterial stiffness.
Increased arterial stiffness is associated with increased risk of cardiovascular complications,16, 17, 18, 19, 20, 21, 22 and a strong correlation between arterial stiffness and the development of atherosclerosis at various sites in arteries has been noted.139, 140 Therefore, measuring arterial stiffness can be a useful clinical tool for disease progression and monitoring of treatment efficacy, as recommended by the European Network for Non-invasive Investigation of Large Arteries15 and the 2007 European guidelines for the management of arterial hypertension.16 The use of arterial stiffness measurements may be particularly useful in assessing endothelial damage induced by certain cardiovascular risk factors, such as cigarette smoking. cfPWV, the ‘gold standard’ for the assessment of aortic stiffness,15, 16 has been used in numerous longitudinal studies, and has the greatest amount of epidemiological evidence to support its predictive value for cardiovascular events in the general and diseased populations.15, 16, 17, 18, 19, 20, 141, 142, 143, 144, 145 Therefore, cfPWV should be the first choice in the assessment of arterial stiffness.
At present, 28% of European adults smoke,146 19% of the Canadian population aged 15 years and older are smokers,2 and 21% of adults in the United States smoke;147 this represents significant proportions of these populations. Moreover, although the general population smoking rates have been declining recently, young people seem to be picking up the habit; 20% of the youth smoked in Europe between the years 1999 and 2001, that number increased to 24% between 2002 and 2005.146 A similar trend exists in Canada; the percentage of smokers in individuals aged 20–24 years is now 28%, up from 24% in 2007.2 It is clear that smoking still represents a significant public health problem in North America and Europe, and the use of arterial stiffness assessments to monitor cardiovascular damage may be valuable from a clinical point of view. In addition, arterial stiffness measurements can also be used to assess the effectiveness of smoking cessation therapies, as well as the direct effect of the smoking cessation medications on arterial stiffness.
At present, there are several pharmacological options for smoking cessation available, such as nicotine replacement therapy (NRT),148, 149 which can help people increase their chances of successfully stopping smoking by 50–70%.148, 150 The market for over-the-counter nicotine gum, which is the most popular form of NRT, had annual sales of more than $300 million at the end of September 2008 in the United States (http://us.infores.com). Although the use of nicotine gum is approved by the Food and Drug Administration and widely advertised, there is no evidence in the literature regarding its direct effect on arterial stiffness. However, it has been shown that administration of nicotine can increase arterial stiffness acutely.55, 151 Therefore, it is possible (although not yet studied) that NRT increases arterial stiffness for the duration of therapy. It is also possible that non-NRT smoking cessation options may not have these effects and thus may be more beneficial. However, these effects of NRT and non-NRT smoking options have yet to be investigated; future research needs to focus on the extent to which smoking cessation therapies (NRT and non-NRT) can lead to stabilization or even reversal of arterial stiffness.
To our knowledge, this is the first systematic review on the effect of smoking on arterial stiffness. We presented results obtained from 39 studies evaluating the effect of acute, chronic and passive smoking on arterial stiffness, and the reversibility of arterial stiffness after smoking cessation. Acute, chronic and passive smoking all have a detrimental effect on arterial stiffness, although the role of chronic smoking in increasing arterial stiffness is slightly more controversial. Chronic smoking was also shown to have a role in sensitizing arterial response to acute smoking. However, whether arterial stiffness is reversed after smoking cessation, and the timeline in which this occurs could not be determined from the available literature. Long-term longitudinal studies using the best recognized parameters of arterial stiffness (cfPWV and AIx) are required to clarify this issue. Furthermore, with the large number of pharmacological options for smoking cessation available, it will become important to identify the direct effect of these medications on arterial stiffness.
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Doonan, R., Hausvater, A., Scallan, C. et al. The effect of smoking on arterial stiffness. Hypertens Res 33, 398–410 (2010). https://doi.org/10.1038/hr.2010.25
- arterial stiffness
- pulse wave velocity
- smoking cessation
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