Elsevier

Toxicology Letters

Volume 215, Issue 1, 23 November 2012, Pages 70-75
Toxicology Letters

Acute toxicant exposure and cardiac autonomic dysfunction from smoking a single narghile waterpipe with tobacco and with a “healthy” tobacco-free alternative

https://doi.org/10.1016/j.toxlet.2012.09.026Get rights and content

Abstract

Tobacco smoking using a waterpipe (narghile, hookah, shisha) has become a global epidemic. Unlike cigarette smoking, little is known about the health effects of waterpipe use. One acute effect of cigarette smoke inhalation is dysfunction in autonomic regulation of the cardiac cycle, as indicated by reduction in heart rate variability (HRV). Reduced HRV is implicated in adverse cardiovascular health outcomes, and is associated with inhalation exposure-induced oxidative stress. Using a 32 participant cross-over study design, we investigated toxicant exposure and effects of waterpipe smoking on heart rate variability when, under controlled conditions, participants smoked a tobacco-based and a tobacco-free waterpipe product promoted as an alternative for “health-conscious” users. Outcome measures included HRV, exhaled breath carbon monoxide (CO), plasma nicotine, and puff topography, which were measured at times prior to, during, and after smoking. We found that waterpipe use acutely decreased HRV (p < 0.01 for all measures), independent of product smoked. Plasma nicotine, blood pressure, and heart rate increased only with the tobacco-based product (p < 0.01), while CO increased with both products (p < 0.01). More smoke was inhaled during tobacco-free product use, potentially reflecting attempted regulation of nicotine intake. The data thus indicate that waterpipe smoking acutely compromises cardiac autonomic function, and does so through exposure to smoke constituents other than nicotine.

Highlights

► Waterpipe tobacco smoking acutely suppresses heart rate variability and increases BP. ► Herbal products exert similar effects on heart rate variability as tobacco products. ► Herbal products result in no nicotine, but similar CO exposure to tobacco products. ► Users draw larger puffs with herbal products, suggesting nicotine compensation.

Introduction

Globally, tobacco use accounts for approximately 5 million deaths per year, mainly due to the use of cigarettes. The causal link between cigarette smoking and early death and disease has long been known, but the health effects of other methods of using tobacco are less well studied, including tobacco smoking through a waterpipe (aka shisha, hookah, narghile). Though centuries old, the practice of waterpipe tobacco smoking (WTS) has exploded in popularity since the early 1990s, particularly among youth (Grekin and Ayna, 2012). Traditionally associated with cultures of Southwest Asia and North Africa, where reported current use rates in various populations now range from 20 to 45% (Saade et al., 2009, Almerie et al., 2008, Azab et al., 2010), surveys in Canada (Roskin and Aveyard, 2009), Estonia (Pärna et al., 2008), Denmark (Jensen et al., 2010), and South Africa (Combrink et al., 2010) indicate that there is a growing worldwide epidemic of WTS (Martinasek et al., 2011). The United States (U.S.) is not immune. Among 105,000 U.S. university students surveyed in 2008, 30% reported “ever use” of a waterpipe to smoke tobacco, and WTS was the second most commonly reported tobacco use method (cigarettes were first; Primack et al., in press). WTS is also reported by U.S. adolescents; in a nationwide sample of 14,900 U.S. 12th graders, 18.5% reported past-year WTS (Johnston et al., 2011).

WTS involves the use of burning charcoal, often in conjunction with a flavored tobacco-based mixture known as ma’assel (Fig. 1). When a user puffs from the mouthpiece, air is drawn through and heated by the charcoal and into the tobacco product to produce smoke. The smoke therefore comprises fumes emanating from both the charcoal and the tobacco, and contains polycyclic aromatic hydrocarbons (PAHs), volatile aldehydes, carbon monoxide (CO), nitric oxide(NO), nicotine, furans, and nanoparticles (Daher et al., 2010, Katurji et al., 2010, Monn et al., 2007, Schubert et al., 2011, Schubert et al., 2012, Shihadeh et al., 2012). Carboxyhemoglobin and plasma nicotine levels rise during waterpipe use (Blank et al., 2011) and metabolites of PAH and tobacco specific nitrosamines can be measured in the urine of waterpipe smokers (Jacob et al., 2011). Thus, waterpipe tobacco smoke contains toxicants to which users are exposed systemically. Not surprisingly then, like cigarette smoking, WTS has been linked to reduced birth weight (Nuwayhid et al., 1998), genetic damage (Khabour et al., 2011), and respiratory disease (Al Mutairi et al., 2006, Raad et al., 2011).

In addition to these and other diseases, cigarette smoking – even smoking a single cigarette – acutely compromises autonomic nervous system (ANS) cardiac control. A non-invasive measure of ANS dysfunction is reduced heart rate variability (HRV), the variation in time between successive heart beats during a given measurement period. In a healthy individual at rest, variation in HRV reflects the normal response of the ANS to continuously vary signaling mechanisms in the body (Dinas et al., in press). Decreases in HRV predict risk of coronary heart disease and mortality (Tsuji et al., 1996, Dekker et al., 2000), are associated with increased systemic inflammation (von Känel et al., 2011), and are associated with an increase in arrhythmia susceptibility after short-term second-hand smoke exposure (Chen et al., 2008). While its clinical interpretations remain a subject of research, HRV as an indicator of ANS cardiac function is widely used in the exposure sciences as a biomarker of environmental insult (Brook et al., 2010).

The hyper-acute effects of cigarette smoking on reducing HRV (Hayano et al., 1990, Karakaya et al., 2007, Kobayashi et al., 2005) are normally attributed to nicotine in up-regulating catecholamine release (Dinas et al., in press). However, respirable particles and other combustion-derived components in cigarette smoke may also reduce HRV (Dinas et al., in press), and may do so through pathways active in acutely reducing HRV in humans and animals exposed to concentrated urban air pollutants (Peters and Pope, 2002, Rodriguez Ferreira Rivero et al., 2005, Chen et al., 2008, Min et al., 2009, Riojas-Rodríguez et al., 2006). Thus, WTS, that also involves inhalation of large quantities of a variety of combustion-derived constituents, may also influence HRV acutely, and may do so independently of the nicotine pathway.

To the best of our knowledge, no study to date has investigated influences of waterpipe smoking on HRV. In this report we describe measurements made of acute changes in HRV, plasma nicotine, and CO associated with a waterpipe use episode. In addition, we compared the acute effects of smoking a waterpipe loaded with tobacco with those of smoking a tobacco-free “herbal” mixture that is advertised as a product for the “health-conscious” waterpipe user (http://www.soex.com/e/herbalmolasses.html). This product does not deliver nicotine (Blank et al., 2011), but like its tobacco-based counterpart, its smoke contains “tar”, CO, NO, PAH, and volatile aldehydes (Shihadeh et al., 2012). We hypothesized that smoking a waterpipe, like cigarette smoking, would reduce HRV and that this influence would be independent of the nicotine delivery of the product smoked in the waterpipe.

Measures of HRV used in this study included low frequency power (LF), high frequency power (HF), and sample entropy (SampEn; Richman and Moorman, 2000). LF and HF are computed using spectral analysis of interbeat (R to R wave) intervals. While HF is commonly accepted as a measure of parasympathetic autonomic system activity, interpretation of LF has been controversial. Conventionally used as a quantitative marker of sympathetic nervous system activation, mounting evidence supports the notion that it reflects baroreflex modulation of cardiac ANS outflows (Rahman et al., 2011). Following the conventional view of LF, the ratio LF/HF is often interpreted as a measure of sympatho/vagal balance (Task Force, 1996), with greater LF/HF indicating dominance of the sympathetic activity, which, in turn is suspected to increase susceptibility to adverse cardiac outcomes (e.g. arrhythmia and sudden cardiac death; Chen et al., 2008). SampEn is a measure of the complexity (or irregularity) of the interbeat interval record, with lower entropy indicating suppressed ANS cardiac regulation. A highly regular record (e.g. indicating failure of the ANS) will result in a computed SampEn value close to zero while a highly irregular record will have a value close to 2. Previous studies have shown that low heart rate entropy is associated with onset of adverse cardiac events in various populations and, conversely, that complexity increases with physical resistance training in healthy men (Huikuri et al., 2009). We note that while the physiological and clinical significance of the various HRV measures remain subjects of ongoing research, the focus of this study is whether inhalation exposure to waterpipe smoke interferes with the cardiac ANS.

Section snippets

Participants

Thirty-three participants recruited in 2010–2011 in Richmond VA provided informed consent and attended at least one session in this Virginia Commonwealth University IRB-approved study. One participant was discontinued for high blood pressure at the beginning of a session. The remaining 32 participants (16 men, 22 non-White) were healthy, aged 18–50 years (M = 21.6 years, SD = 2.7), reported smoking tobacco using a waterpipe at least four times per month (M = 11.4, SD = 10.9) for the past six months (M = 

Plasma nicotine/expired air CO exposure and puff topography

Table 1 shows the mean plasma nicotine, expired air CO, and puff topography data for the tobacco and tobacco-free conditions. As can be seen, plasma nicotine levels were elevated in the tobacco condition only, and significantly greater expired air CO levels were observed in the tobacco-free condition (p < 0.01). For the tobacco condition, peak plasma nicotine and peak CO were highly correlated (N = 29; r = 0.751, p < 0.01). Peak plasma nicotine concentrations were also compared between waterpipe

Discussion

Acute and/or chronic inhalation of airborne particle pollutants is widely recognized as a factor in cardiovascular-related morbidity and mortality. Central hypotheses in the pathophysiology of airborne particulate matter-related cardiovascular disease include instigation of proinflammatory responses, alterations in systemic ANS activity, and direct effects of particulate matter constituents on airway receptors and in the systemic circulation (Brook et al., 2010, Routledge et al., 2006). These

Conclusions

A single waterpipe use session leads to measurable transient dysfunction in cardiac autonomic regulation, and suggests an increased risk of adverse cardiac events in users. Cardiac regulation is compromised with both tobacco-based and tobacco-free “herbal” waterpipe products, and therefore effects on HRV cannot be ascribed to effects of nicotine, although other known effects of nicotine (increase in HR) were observed only when participants smoked the nicotine-containing products. In addition to

Funding

This work is supported by U.S. Public Health Service Grants R01CA120142, R01DA025659, and F31DA028102.

Conflict of interest

The authors declare that there are no conflicts of interest

Acknowledgements

The authors thank Mr. Ezzat Jaroudi, M.Eng. of the AUB for programming the data acquisition device, and Barbara Kilgalen, R.N., and Janet Austin, M.S. of VCU for their diligent efforts on data collection and management. Some of the data presented here were presented at the 73rd annual meeting of the College on Problems of Drug Dependence, and are part of a doctoral dissertation completed by Caroline O. Cobb at Virginia Commonwealth University.

References (50)

  • A. Shihadeh

    Investigation of the mainstream smoke aerosol of the argileh water pipe

    Food and Chemical Toxicology

    (2003)
  • A. Shihadeh et al.

    Does switching to a tobacco-free waterpipe product reduce toxicant intake? A crossover study comparing CO, NO, PAH, volatile aldehydes, “tar” and nicotine yields

    Food and Chemical Toxicology

    (2012)
  • R.M. Wolfram et al.

    Narghile (water pipe) smoking influences platelet function and (iso-)eicosanoids

    Life Sciences

    (2003)
  • M.Q. Almerie et al.

    Cigarettes and waterpipe smoking among medical students in Syria: a cross-sectional study

    International Journal of Tuberculosis and Lung Disease

    (2008)
  • S.S. Al Mutairi et al.

    Comparative analysis of the effects of hubble-bubble (Sheesha) and cigarette smoking on respiratory and metabolic parameters in hubble-bubble and cigarette smokers

    Respirology

    (2006)
  • M. Azab et al.

    Waterpipe tobacco smoking among university students in Jordan

    Nicotine and Tobacco Research

    (2010)
  • B. Baldinger et al.

    Effects of smoking abstinence and nicotine abstinence on heart rate, activity and cigarette craving under field conditions

    Human Psychopharmacology

    (1995)
  • A.B. Breland et al.

    Clinical laboratory evaluation of potential reduced exposure products for smokers

    Nicotine and Tobacco Research

    (2006)
  • R.D. Brook et al.

    Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association

    Circulation

    (2010)
  • R.D. Brook et al.

    Air pollution and cardiovascular disease. A statement for healthcare professionals from the expert panel on population and prevention science of the American Heart Association

    Circulation

    (2004)
  • C.Y. Chen et al.

    Short-term secondhand smoke exposure decreases heart rate variability and increases arrhythmia susceptibility in mice

    American Journal of Physiology: Heart and Circulatory Physiology

    (2008)
  • Cobb, C.O., 2012. Evaluating the acute effects of caffeinated waterpipe tobacco in waterpipe users. Doctoral...
  • A. Combrink et al.

    High prevalence of hookah smoking among secondary school students in a disadvantaged community in Johannesburg

    South African Medical Journal

    (2010)
  • J.M. Dekker et al.

    Low heart rate variability in a 2-minute rhythm strip predicts risk of coronary heart disease and mortality from several causes: the ARIC study

    Circulation

    (2000)
  • Dinas, P.C., Koutedakis, Y., Flouris, A.D., 2011. Effects of active and passive tobacco cigarette smoking on heart rate...
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