Overt and Latent Cardiac Effects of Ozone Inhalation in Rats: Evidence for Autonomic Modulation and Increased Myocardial Vulnerability

By Farraj, Aimen K.; Hazari, Mehdi S. et al. | Environmental Health Perspectives, March 2012 | Go to article overview

Overt and Latent Cardiac Effects of Ozone Inhalation in Rats: Evidence for Autonomic Modulation and Increased Myocardial Vulnerability


Farraj, Aimen K., Hazari, Mehdi S., Winsett, Darrell W., Kulukuiualani, Anthony, Carll, Alex P., Haykal-Coates, Najwa, Lamb, Christina M., Lappi, Edwin, Terrell, Dock, Cascio, Wayne E., Costa, Daniel L., Environmental Health Perspectives


BACKGROUND: Ozone ([O.sub.3]) is a well-documented respiratory oxidant but increasing epidemiological evidence points to extrapulmonary effects, including positive associations between ambient [O.sub.3] concentrations and cardiovascular morbidity and mortality.

OBJECTIVE; With preliminary reports linking [O.sub.3] exposure with changes in heart rate (HR), we investigated the hypothesis that a single inhalation exposure to [O.sub.3] will cause concentration-dependent autonomic modulation of cardiac function in rats.

METHODS: Rats implanted with telemeters to monitor HR and cardiac electrophysiology [electrocardiography (ECG)] were exposed once by whole-body inhalation for 4 hr to 0.2 or 0.8 ppm [O.sub.3] or filtered air. A separate cohort was tested for vulnerability to aconitine-induced arrhythmia 24 hr after exposure.

RESULTS: Exposure to 0.8 ppm [O.sub.3] caused bradycardia, PR prolongation, ST depression, and substantial increases in atrial premature beats, sinoatrial block, and atrioventricular block, accompanied by concurrent increases in several HR variability parameters that were suggestive of increased parasympathetic tone. Low-03 exposure failed to elicit any overt changes in autonomic tone, heart rhythm, or ECG. However, both 0.2 and 0.8 ppm [O.sub.3] increased sensitivity to aconitine-induced arrhythmia formation, suggesting a latent [O.sub.3]-induced alteration in myocardial excitability.

CONCLUSIONS: [O.sub.3] exposure causes several alterations in cardiac electrophysiology that are likely mediated by modulation of autonomic input to the heart. Moreover, exposure to low [O.sub.3] concentrations may cause subclinical effects that manifest only when triggered by a stressor, suggesting that the adverse health effects of ambient levels of air pollutants may be insidious and potentially under-estimated.

KEY WORDS: air pollution, arrhythmia, autonomic, cardiac, electrocardiogram, heart rate variability, inhalation, latent, overt, ozone, rats. Environ Health Perspect 120:348-354 (2012). http://dx.doi. org/10.1289/ehp.l 104244 [Online 2 December 2011]

Ozone ([O.sub.3]) is a major smog-associated oxidant with well-established respiratory effects, including decrements in lung function, airway injury and inflammation, compromised host defense, and asthma exacerbation (Hollingsworth et al. 2007; Mudway and Kelly 2000). Although the lung has understandably been the target organ of interest, recent epidemiological evidence suggests a positive association between inhaled [O.sub.3] and clinical cardiovascular events linked to coronary artery disease, myocardial infarction, and atherosclerosis (Srcbot et al 2009); these effects are largely independent of exposure to other pollutants. In controlled human exposure studies, [O.sub.3] exposure has reduced maximal oxygen uptake (Gong et al 1998) and, in combination with ambient particulate matter (PM), increased diastolic blood pressure (Fakhri et al. 2009) and caused arterial vasoconstriction (Brook et al 2002). Adverse cardiovascular effects, including increased atherosclerotic plaque size (Chuang et al. 2009) and enhanced sensitivity to ischemic injury (Perepu et al. 2010), have also been reported in animal models.

Upon inhalation, [O.sub.3] is thought to oxidate or pcroxidate biological molecules (directly or indirectly) at the surface of the respiratory tract, triggering a pathological cascade characterized by lipid peroxidation, enzyme inactivation, free radical formation, altered membrane permeability, and inflammation (Mustafa 1990). Less is known, however, about the mechanisms mediating [O.sub.3]-induced cardiovascular responses and the potential influence of [O.sub.3]-induced respiratory effects on cardiovascular function. Although preliminary, the available evidence implicates the following mechanisms: vascular oxidative stress, endothelial/vascular dysfunction, inflammation, and altered autonomic tone (Srebotetal. …

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