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Inhalation of diluted diesel engine emission impacts heart rate variability and arrhythmia occurrence in a rat model of chronic ischemic heart failure

  • Organ Toxicity and Mechanisms
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Abstract

Both increase in cardiac arrhythmia incidence and decrease in heart rate variability (HRV) have been described following human and experimental animal exposures to air pollutants. However, the potential causal relationship between these two factors remains unclear. Incidence of ventricular arrhythmia and HRV were evaluated during and after a 3 h period of Diesel engine exhaust exposure in ten healthy and ten chronic ischemic heart failure (CHF, 3 months after coronary ligation) Wistar rats using implantable ECG telemetry. Air pollutants were delivered to specifically designed whole body individual exposure chambers at particulate matter concentrations similar to those measured inside cabins of cars inserted in congested urban traffic. Recordings were obtained from unrestraint and unsedated vigil rats. Immediate decrease in RMSSD was observed in both healthy (6.64 ± 2.62 vs. 4.89 ± 1.67 ms, P < 0.05) and CHF rats (8.01 ± 0.89 vs. 6.6 ± 1.37 ms, P < 0.05) following exposure. An immediate 200–500% increase in ventricular premature beats was observed in CHF rats only. Whereas HRV progressively returned to baseline values within 2.5 h after exposure start, the proarrhythmic effect persisted as late as 5 h after exposure termination in CHF rats. Persistence of ventricular proarrhythmic effects after HRV normalization suggests that HRV reduction is not the mechanism of cardiac arrhythmias in this model. Our methodological approach, closely reflecting the real clinical situations, appeared to be a unique tool to provide further insight into the pathophysiological mechanisms of traffic related airborne pollution health impact.

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Abbreviations

CHF:

Chronic heart failure (at least 3 months after left coronary artery ligation)

ECG:

Electrocardiogram

HRV:

Heart rate variability

RMSSD:

The square root of the mean squared differences of successive sinusal beats

SDNN:

Standard deviation of sinusal beat-to-beat intervals

SMPS:

Scanning mobility particle sizer (apparatus measuring particle number and size distribution)

References

  • Bion A, Fall M, Gouriou F, Le Prieur E, Dionnet F, Morin JP (2002) Biphasic culture of rat lung slices for pharmacotoxicological evaluation of complex atmospheres. Cell Biol Toxicol 18:301–314

    Article  PubMed  CAS  Google Scholar 

  • Campen MJ, Nolan JP, Schladweiler MC, Kodavanti UP, Costa DL, Watkinson WP (2002) Cardiac and thermoregulatory effects of instilled particulate matter-associated transition metals in healthy and cardiopulmonary-compromised rats. Toxicol Environ Health A 65(20):1615–1631

    Article  CAS  Google Scholar 

  • Campen MJ, McDonald JD, Gigliotti AP, Seilkop SK, Reed MD, Benson JM (2003) Cardiovascular effects of inhaled diesel exhaust in spontaneously hypertensive rats. Cardiovasc Toxicol 3(4):353–361

    Article  PubMed  CAS  Google Scholar 

  • Chang CC, Hwang JS, Chan CC, Wang PY, Hu TH, Cheng TJ (2004) Effects of concentrated ambient particles on heart rate, blood pressure, and cardiac contractility in spontaneously hypertensive rats. Inhal Toxicol 16(6–7):421–429

    Article  PubMed  CAS  Google Scholar 

  • Devlin RB, Ghio AJ, Kehrl H, Sanders G, Cascio W (2003) Elderly humans exposed to concentrated air pollution particles have decreased heart rate variability. Eur Respir J Suppl 40:76s–80s

    Article  PubMed  CAS  Google Scholar 

  • Goldberg MS, Burnett RT, Bailar JC 3rd, Tamblyn R, Ernst P, Flegel K, Brook J, Bonvalot Y, Singh R, Valois MF, Vincent R (2001) Identification of persons with cardiorespiratory conditions who are at risk of dying from the acute effects of ambient air particles. Environ Health Perspect 109(Suppl 4):487–494

    Article  PubMed  CAS  Google Scholar 

  • Goldberg MS, Burnett RT, Valois MF, Flegel K, Bailar JC 3rd, Brook J, Vincent R, Radon K (2003) Associations between ambient air pollution and daily mortality among persons with congestive heart failure. Environ Res 91(1):8–20

    Article  PubMed  CAS  Google Scholar 

  • Gouriou F, Morin JP, Weill ME (2004) On road measurements of particle number concentrations and size distributions in urban and tunnel environments. Atmos Environ 38:2831–2840

    Article  CAS  Google Scholar 

  • Kelly FJ (2003) Oxidative stress: its role in air pollution and adverse health effects. Occup Environ Med 60:612–616

    Article  PubMed  Google Scholar 

  • Mann JK, Tager IB, Lurmann F, Segal M, Quesenberry CP Jr, Lugg MM, Shan J, Van Den Eeden SK (2002) Air pollution and hospital admissions for ischemic heart disease in persons with congestive heart failure or arrhythmia. Environ Health Perspect 110(12):1247–1252

    PubMed  CAS  Google Scholar 

  • Mulder P, Richard V, Derumeaux G, Hogie M, Henry JP, Lallemand F, Compagnon P, Mace B, Comoy E, Letac B, Thuillez C (1997) Role of endogenous endothelin in chronic heart failure: effect of long-term treatment with an endothelin antagonist on survival, hemodynamics, and cardiac remodeling. Circulation 96(6):1976–1982

    PubMed  CAS  Google Scholar 

  • Mulder P, Barbier S, Chagraoui A, Richard V, Henry JP, Lallemand F, Renet S, Lerebours G, Mahlberg-Gaudin F, Thuillez C (2004) Long-term heart rate reduction induced by the selective I(f) current inhibitor ivabradine improves left ventricular function and intrinsic myocardial structure in congestive heart failure. Circulation 109(13):1674–1679

    Article  PubMed  CAS  Google Scholar 

  • Nadziejko C, Fang K, Narciso S, Zhong M, Su WC, Gordon T, Nadas A, Chen LC (2004) Effect of particulate and gaseous pollutants on spontaneous arrhythmias in aged rats. Inhal Toxicol 16(6–7):373–380

    Article  PubMed  CAS  Google Scholar 

  • Nemmar A, Hoet M, Vanquickenborne B, Dinsdale D, Thomeer M, Hoylaerts MF, Vanbilloen H, Mortelmans L, Nemery B (2002a) Passage of inhaled particles into the blood circulation in humans. Circulation 105:411–414

    Article  CAS  Google Scholar 

  • Nemmar A, Hoylaerts MF, Hoet PH, Dinsdale D, Smith T, Xu H, Vermylen J, Nemery B (2002b) Ultrafine particles affect experimental thrombosis in an in vivo hamster model. Am J Respir Crit Care Med 166(7):998–1004

    Article  Google Scholar 

  • Nemmar A, Hoet PH, Dinsdale D, Vermylen J, Hoylaerts MF, Nemery B (2003) Diesel exhaust particles in lung acutely enhance experimental peripheral thrombosis. Circulation 107(8):1202–1208

    Article  PubMed  Google Scholar 

  • Peters A, Liu E, Verrier RL, Schwartz J, Gold DR, Mittleman M, Baliff J, Oh JA, Allen G, Monahan K, Dockery DW (2000) Air pollution and incidence of cardiac arrhythmia. Epidemiology 11(1):11–17

    Article  PubMed  CAS  Google Scholar 

  • Pfeffer MA, Pfeffer JM, Steinberg C, Finn P (1985) Survival after an experimental myocardial infarction: beneficial effects of long-term therapy with captopril. Circulation 72(2):406–412

    PubMed  CAS  Google Scholar 

  • Pope CA 3rd, Burnett RT, Thurston GD, Thun MJ, Calle EE, Krewski D, Godleski JJ (2004a) Cardiovascular mortality and long-term exposure to particulate air pollution: epidemiological evidence of general pathophysiological pathways of disease. Circulation 109(1):71–77

    Article  Google Scholar 

  • Pope CA 3rd, Hansen ML, Long RW, Nielsen KR, Eatough NL, Wilson WE, Eatough DJ (2004b) Ambient particulate air pollution, heart rate variability, and blood markers of inflammation in a panel of elderly subjects. Environ Health Perspect 112(3):339–345

    Article  Google Scholar 

  • Salvi S, Blomberg A, Rudell B, Kelly F, sandstorm T, Holgate ST, Frew A (1999) Acute inflammatory responses in the airways and peripheral blood after short-term exposure to diesel exhaust in healthy human volunteers. Am J Respir Crit Care Med 159:702–709

    PubMed  CAS  Google Scholar 

  • Samet JM, Dominici F, Curriero FC, Coursac I, Zeger SL (2000) Fine particulate air pollution and mortality in 20 US cities, 1987–1994. N Engl J Med 343(24):1742–1749

    Article  PubMed  CAS  Google Scholar 

  • Samoli E, Aga E, Touloumi G, Nisiotis K, Forsberg B, Lefranc A, Pekkanen J, Wojtyniak B, Schindler C, Niciu E, Brunstein R, Dodic Fikfak M, Schwartz J, Katsouyanni K (2006) Short-term effects of nitrogen dioxide on mortality: an analysis within the APHEA project. Eur Respir J 27:1129–1137

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JH, Schreuder AB, Trenga CA, Liu SL, Larson TV, Koenig JQ, Kaufman JD (2005) Association between short term exposure to fine particulate matter and heart rate variability in older subjects with and without heart disease. Thorax 60(6):462–466

    Article  PubMed  CAS  Google Scholar 

  • Task Force European Society Cardiology (1996) Heart rate Variability: standards of measurements, physiological interpretations and clinical use. Circulation 93:1043–1065

    Google Scholar 

  • Von Klot S, Peters A, Aalto P, Bellander T, Berglind N, D’Ippoliti D, Elosua R, Hormann A, Kulmala M, Lanki T, Lowel H, Pekkanen J, Picciotto S, Sunyer J, Forastiere F (2005) Health effects of particles on susceptible subpopulations (HEAPSS) study group. Ambient air pollution is associated with increased risk of hospital cardiac readmissions of myocardial infarction survivors in five European cities. Circulation. 112(20):3073–3079. Erratum in: Circulation 2006 Feb 7;113(5):e71

    Google Scholar 

  • Watkinson WP, Campen MJ, Costa DL (1998) Cardiac arrhythmia induction after exposure to residual oil fly ash particles in a rodent model of pulmonary hypertension. Toxicol Sci 41:209–216

    Article  PubMed  CAS  Google Scholar 

  • Wellenius GA, Saldiva PH, Batalha JR, Krishna Murthy GG, Coull BA, Verrier RL, Godleski JJ (2002) Electrocardiographic changes during exposure to residual oil fly ash (ROFA) particles in a rat model of myocardial infarction. Toxicol Sci 66(2):327–335

    Article  PubMed  CAS  Google Scholar 

  • Wellenius GA, Batalha JR, Diaz EA, Lawrence J, Coull BA, Katz T, Verrier RL, Godleski JJ (2004) Cardiac effects of carbon monoxide and ambient particles in a rat model of myocardial infarction. Toxicol Sci 80(2):367–376

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Financial supports from EC QLK4-CT62002-02357 MAAPHRI program, ADEME, Direction Generale de la Sante and Région Haute Normandie are greatly acknowledged. Dr Konstandopoulos (CERTH Thessaloniki Grece) for fluid dynamics computation and skilled technical assistance from Mrs. Annie Lejeune are greatly acknowledged

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Authors and Affiliations

  1. Service de Cardiologie, Rouen University Hospital, Rouen, France

    Frédéric Anselme

  2. INSERM U644, School of Medicine-Pharmacy, University of Rouen France, 22 bd Gambetta, Rouen, Cedex, 76 183, France

    Stéphane Loriot, Jean-Paul Henry, Christian Thuillez & Jean-Paul Morin

  3. Centre d’Etudes et de Recherches Technologiques en Aérothermique et Moteurs, Saint Etienne du Rouvray, France

    Frédéric Dionnet

  4. EMKA Technologies, Paris, France

    Jean-Gérard Napoleoni

Authors
  1. Frédéric Anselme
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  2. Stéphane Loriot
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  3. Jean-Paul Henry
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  4. Frédéric Dionnet
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  5. Jean-Gérard Napoleoni
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  6. Christian Thuillez
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  7. Jean-Paul Morin
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Correspondence to Jean-Paul Morin.

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Anselme, F., Loriot, S., Henry, JP. et al. Inhalation of diluted diesel engine emission impacts heart rate variability and arrhythmia occurrence in a rat model of chronic ischemic heart failure. Arch Toxicol 81, 299–307 (2007). https://doi.org/10.1007/s00204-006-0147-4

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  • DOI: https://doi.org/10.1007/s00204-006-0147-4

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