Skip to main content
Top
Published in: Cardiovascular Toxicology 2/2017

01-04-2017

Acrolein Inhalation Alters Myocardial Synchrony and Performance at and Below Exposure Concentrations that Cause Ventilatory Responses

Authors: Leslie C. Thompson, Allen D. Ledbetter, Najwa Haykal-Coates, Wayne E. Cascio, Mehdi S. Hazari, Aimen K. Farraj

Published in: Cardiovascular Toxicology | Issue 2/2017

Login to get access

Abstract

Acrolein is an irritating aldehyde generated during combustion of organic compounds. Altered autonomic activity has been documented following acrolein inhalation, possibly impacting myocardial synchrony and function. Given the ubiquitous nature of acrolein in the environment, we sought to better define the immediate and delayed functional cardiac effects of acrolein inhalation in vivo. We hypothesized that acrolein inhalation would increase markers of cardiac mechanical dysfunction, i.e., myocardial dyssynchrony and performance index in mice. Male C57Bl/6J mice were exposed to filtered air (FA) or acrolein (0.3 or 3.0 ppm) for 3 h in whole-body plethysmography chambers (n = 6). Echocardiographic analyses were performed 1 day before exposure and at 1 and 24 h post-exposure. Speckle tracking echocardiography revealed that circumferential strain delay (i.e., dyssynchrony) was increased at 1 and 24 h following exposure to 3.0 ppm, but not 0.3 ppm, when compared to pre-exposure and/or FA exposure. Pulsed wave Doppler of transmitral blood flow revealed that acrolein exposure at 0.3 ppm, but not 3.0 ppm, increased the Tei index of myocardial performance (i.e., decreased global heart performance) at 1 and 24 h post-exposure compared to pre-exposure and/or FA exposure. We conclude that short-term inhalation of acrolein can acutely modify cardiac function in vivo and that echocardiographic evaluation of myocardial synchrony and performance following exposure to other inhaled pollutants could provide broader insight into the health effects of air pollution.
Appendix
Available only for authorised users
Literature
1.
go back to reference Brook, R. D., Rajagopalan, S., Pope, C. A, 3rd, Brook, J. R., Bhatnagar, A., Diez-Roux, A. V., et al. (2010). Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation, 121, 2331–2378.CrossRefPubMed Brook, R. D., Rajagopalan, S., Pope, C. A, 3rd, Brook, J. R., Bhatnagar, A., Diez-Roux, A. V., et al. (2010). Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association. Circulation, 121, 2331–2378.CrossRefPubMed
2.
go back to reference Moghe, A., Ghare, S., Lamoreau, B., Mohammad, M., Barve, S., McClain, C., & Joshi-Barve, S. (2015). Molecular mechanisms of acrolein toxicity: Relevance to human disease. Toxicological Sciences, 143, 242–255.CrossRefPubMedPubMedCentral Moghe, A., Ghare, S., Lamoreau, B., Mohammad, M., Barve, S., McClain, C., & Joshi-Barve, S. (2015). Molecular mechanisms of acrolein toxicity: Relevance to human disease. Toxicological Sciences, 143, 242–255.CrossRefPubMedPubMedCentral
3.
go back to reference EPA. (2003). Toxicological review of acrolein (CAS No. 107-02-8). Washington, DC: US Environmental Protection Agency. EPA. (2003). Toxicological review of acrolein (CAS No. 107-02-8). Washington, DC: US Environmental Protection Agency.
4.
go back to reference ATSDR. (2007). Toxicological profile for acrolein. U.S: Department of Health and Human Services, Public Health Service, Atlanta, GA. ATSDR. (2007). Toxicological profile for acrolein. U.S: Department of Health and Human Services, Public Health Service, Atlanta, GA.
5.
go back to reference Haussmann, H. J. (2012). Use of hazard indices for a theoretical evaluation of cigarette smoke composition. Chemical Research in Toxicology, 25, 794–810.CrossRefPubMed Haussmann, H. J. (2012). Use of hazard indices for a theoretical evaluation of cigarette smoke composition. Chemical Research in Toxicology, 25, 794–810.CrossRefPubMed
7.
go back to reference Perez, C. M., Ledbetter, A. D., Hazari, M. S., Haykal-Coates, N., Carll, A. P., Winsett, D. W., et al. (2013). Hypoxia stress test reveals exaggerated cardiovascular effects in hypertensive rats after exposure to the air pollutant acrolein. Toxicological Sciences, 132, 467–477.CrossRefPubMedPubMedCentral Perez, C. M., Ledbetter, A. D., Hazari, M. S., Haykal-Coates, N., Carll, A. P., Winsett, D. W., et al. (2013). Hypoxia stress test reveals exaggerated cardiovascular effects in hypertensive rats after exposure to the air pollutant acrolein. Toxicological Sciences, 132, 467–477.CrossRefPubMedPubMedCentral
8.
go back to reference Hazari, M. S., Griggs, J., Winsett, D. W., Haykal-Coates, N., Ledbetter, A., Costa, D. L., & Farraj, A. K. (2014). A single exposure to acrolein desensitizes baroreflex responsiveness and increases cardiac arrhythmias in normotensive and hypertensive rats. Cardiovascular Toxicology, 14, 52–63.CrossRefPubMed Hazari, M. S., Griggs, J., Winsett, D. W., Haykal-Coates, N., Ledbetter, A., Costa, D. L., & Farraj, A. K. (2014). A single exposure to acrolein desensitizes baroreflex responsiveness and increases cardiac arrhythmias in normotensive and hypertensive rats. Cardiovascular Toxicology, 14, 52–63.CrossRefPubMed
9.
go back to reference Luo, J., Hill, B. G., Gu, Y., Cai, J., Srivastava, S., Bhatnagar, A., & Prabhu, S. D. (2007). Mechanisms of acrolein-induced myocardial dysfunction: Implications for environmental and endogenous aldehyde exposure. American Journal of Physiology Heart and Circulatory Physiology, 293, H3673–H3684.CrossRefPubMed Luo, J., Hill, B. G., Gu, Y., Cai, J., Srivastava, S., Bhatnagar, A., & Prabhu, S. D. (2007). Mechanisms of acrolein-induced myocardial dysfunction: Implications for environmental and endogenous aldehyde exposure. American Journal of Physiology Heart and Circulatory Physiology, 293, H3673–H3684.CrossRefPubMed
10.
go back to reference Wang, L., Sun, Y., Asahi, M., & Otsu, K. (2011). Acrolein, an environmental toxin, induces cardiomyocyte apoptosis via elevated intracellular calcium and free radicals. Cell Biochemistry and Biophysics, 61, 131–136.CrossRefPubMed Wang, L., Sun, Y., Asahi, M., & Otsu, K. (2011). Acrolein, an environmental toxin, induces cardiomyocyte apoptosis via elevated intracellular calcium and free radicals. Cell Biochemistry and Biophysics, 61, 131–136.CrossRefPubMed
11.
go back to reference Wu, Z., He, E. Y., Scott, G. I., & Ren, J. (2015). Alpha, beta-unsaturated aldehyde pollutant acrolein suppresses cardiomyocyte contractile function: Role of TRPV1 and oxidative stress. Environmental Toxicology, 30, 638–647.CrossRefPubMed Wu, Z., He, E. Y., Scott, G. I., & Ren, J. (2015). Alpha, beta-unsaturated aldehyde pollutant acrolein suppresses cardiomyocyte contractile function: Role of TRPV1 and oxidative stress. Environmental Toxicology, 30, 638–647.CrossRefPubMed
12.
go back to reference Stypmann, J., Engelen, M. A., Troatz, C., Rothenburger, M., Eckardt, L., & Tiemann, K. (2009). Echocardiographic assessment of global left ventricular function in mice. Laboratory Animals, 43, 127–137.CrossRefPubMed Stypmann, J., Engelen, M. A., Troatz, C., Rothenburger, M., Eckardt, L., & Tiemann, K. (2009). Echocardiographic assessment of global left ventricular function in mice. Laboratory Animals, 43, 127–137.CrossRefPubMed
13.
go back to reference Dandel, M., Lehmkuhl, H., Knosalla, C., Suramelashvili, N., & Hetzer, R. (2009). Strain and strain rate imaging by echocardiography—Basic concepts and clinical applicability. Current Cardiology Reviews, 5, 133–148.CrossRefPubMedPubMedCentral Dandel, M., Lehmkuhl, H., Knosalla, C., Suramelashvili, N., & Hetzer, R. (2009). Strain and strain rate imaging by echocardiography—Basic concepts and clinical applicability. Current Cardiology Reviews, 5, 133–148.CrossRefPubMedPubMedCentral
14.
go back to reference Thavendiranathan, P., Poulin, F., Lim, K. D., Plana, J. C., Woo, A., & Marwick, T. H. (2014). Use of myocardial strain imaging by echocardiography for the early detection of cardiotoxicity in patients during and after cancer chemotherapy: A systematic review. Journal of the American College of Cardiology, 63, 2751–2768.CrossRefPubMed Thavendiranathan, P., Poulin, F., Lim, K. D., Plana, J. C., Woo, A., & Marwick, T. H. (2014). Use of myocardial strain imaging by echocardiography for the early detection of cardiotoxicity in patients during and after cancer chemotherapy: A systematic review. Journal of the American College of Cardiology, 63, 2751–2768.CrossRefPubMed
15.
go back to reference Tei, C., Ling, L. H., Hodge, D. O., Bailey, K. R., Oh, J. K., Rodeheffer, R. J., et al. (1995). New index of combined systolic and diastolic myocardial performance: A simple and reproducible measure of cardiac function—a study in normals and dilated cardiomyopathy. Journal of Cardiology, 26, 357–366.PubMed Tei, C., Ling, L. H., Hodge, D. O., Bailey, K. R., Oh, J. K., Rodeheffer, R. J., et al. (1995). New index of combined systolic and diastolic myocardial performance: A simple and reproducible measure of cardiac function—a study in normals and dilated cardiomyopathy. Journal of Cardiology, 26, 357–366.PubMed
16.
go back to reference Caro, A. C., Hankenson, F. C., & Marx, J. O. (2013). Comparison of thermoregulatory devices used during anesthesia of C57BL/6 mice and correlations between body temperature and physiologic parameters. Journal of the American Association for Laboratory Animal Science, 52, 577–583.PubMedPubMedCentral Caro, A. C., Hankenson, F. C., & Marx, J. O. (2013). Comparison of thermoregulatory devices used during anesthesia of C57BL/6 mice and correlations between body temperature and physiologic parameters. Journal of the American Association for Laboratory Animal Science, 52, 577–583.PubMedPubMedCentral
17.
go back to reference Jaskot, R. H., Charlet, E. G., Grose, E. C., Grady, M. A., & Roycroft, J. H. (1983). An automated analysis of glutathione peroxidase, S-transferase, and reductase activity in animal tissue. Journal of Analytical Toxicology, 7, 86–88.CrossRefPubMed Jaskot, R. H., Charlet, E. G., Grose, E. C., Grady, M. A., & Roycroft, J. H. (1983). An automated analysis of glutathione peroxidase, S-transferase, and reductase activity in animal tissue. Journal of Analytical Toxicology, 7, 86–88.CrossRefPubMed
18.
go back to reference Perez, C. M., Hazari, M. S., Ledbetter, A. D., Haykal-Coates, N., Carll, A. P., Cascio, W. E., et al. (2015). Acrolein inhalation alters arterial blood gases and triggers carotid body-mediated cardiovascular responses in hypertensive rats. Inhalation Toxicology, 27, 54–63.CrossRefPubMedPubMedCentral Perez, C. M., Hazari, M. S., Ledbetter, A. D., Haykal-Coates, N., Carll, A. P., Cascio, W. E., et al. (2015). Acrolein inhalation alters arterial blood gases and triggers carotid body-mediated cardiovascular responses in hypertensive rats. Inhalation Toxicology, 27, 54–63.CrossRefPubMedPubMedCentral
19.
go back to reference Shen, M. J., & Zipes, D. P. (2014). Role of the autonomic nervous system in modulating cardiac arrhythmias. Circulation Research, 114, 1004–1021.CrossRefPubMed Shen, M. J., & Zipes, D. P. (2014). Role of the autonomic nervous system in modulating cardiac arrhythmias. Circulation Research, 114, 1004–1021.CrossRefPubMed
20.
go back to reference Paton, J. F., Boscan, P., Pickering, A. E., & Nalivaiko, E. (2005). The yin and yang of cardiac autonomic control: Vago-sympathetic interactions revisited. Brain Research. Brain Research Reviews, 49, 555–565.CrossRefPubMed Paton, J. F., Boscan, P., Pickering, A. E., & Nalivaiko, E. (2005). The yin and yang of cardiac autonomic control: Vago-sympathetic interactions revisited. Brain Research. Brain Research Reviews, 49, 555–565.CrossRefPubMed
21.
go back to reference Gimelli, A., Liga, R., Genovesi, D., Giorgetti, A., Kusch, A., & Marzullo, P. (2014). Association between left ventricular regional sympathetic denervation and mechanical dyssynchrony in phase analysis: A cardiac CZT study. European Journal of Nuclear Medicine and Molecular Imaging, 41, 946–955.CrossRefPubMed Gimelli, A., Liga, R., Genovesi, D., Giorgetti, A., Kusch, A., & Marzullo, P. (2014). Association between left ventricular regional sympathetic denervation and mechanical dyssynchrony in phase analysis: A cardiac CZT study. European Journal of Nuclear Medicine and Molecular Imaging, 41, 946–955.CrossRefPubMed
22.
go back to reference Schlack, W., Schafer, S., & Thamer, V. (1994). Left stellate ganglion block impairs left ventricular function. Anesthesia and Analgesia, 79, 1082–1088.CrossRefPubMed Schlack, W., Schafer, S., & Thamer, V. (1994). Left stellate ganglion block impairs left ventricular function. Anesthesia and Analgesia, 79, 1082–1088.CrossRefPubMed
23.
go back to reference Schlack, W., & Thamer, V. (1996). Unilateral changes of sympathetic tone to the heart impair left ventricular function. Acta Anaesthesiologica Scandinavica, 40, 262–271.CrossRefPubMed Schlack, W., & Thamer, V. (1996). Unilateral changes of sympathetic tone to the heart impair left ventricular function. Acta Anaesthesiologica Scandinavica, 40, 262–271.CrossRefPubMed
24.
go back to reference Sequeira, I. M., Haberberger, R. V., & Kummer, W. (2005). Atrial and ventricular rat coronary arteries are differently supplied by noradrenergic, cholinergic and nitrergic, but not sensory nerve fibres. Annals of Anatomy, 187, 345–355.CrossRefPubMed Sequeira, I. M., Haberberger, R. V., & Kummer, W. (2005). Atrial and ventricular rat coronary arteries are differently supplied by noradrenergic, cholinergic and nitrergic, but not sensory nerve fibres. Annals of Anatomy, 187, 345–355.CrossRefPubMed
25.
go back to reference Reant, P., Labrousse, L., Lafitte, S., Bordachar, P., Pillois, X., Tariosse, L., et al. (2008). Experimental validation of circumferential, longitudinal, and radial 2-dimensional strain during dobutamine stress echocardiography in ischemic conditions. Journal of the American College of Cardiology, 51, 149–157.CrossRefPubMed Reant, P., Labrousse, L., Lafitte, S., Bordachar, P., Pillois, X., Tariosse, L., et al. (2008). Experimental validation of circumferential, longitudinal, and radial 2-dimensional strain during dobutamine stress echocardiography in ischemic conditions. Journal of the American College of Cardiology, 51, 149–157.CrossRefPubMed
26.
go back to reference Winter, R., Jussila, R., Nowak, J., & Brodin, L. A. (2007). Speckle tracking echocardiography is a sensitive tool for the detection of myocardial ischemia: A pilot study from the catheterization laboratory during percutaneous coronary intervention. Journal of the American Society of Echocardiography, 20, 974–981.CrossRefPubMed Winter, R., Jussila, R., Nowak, J., & Brodin, L. A. (2007). Speckle tracking echocardiography is a sensitive tool for the detection of myocardial ischemia: A pilot study from the catheterization laboratory during percutaneous coronary intervention. Journal of the American Society of Echocardiography, 20, 974–981.CrossRefPubMed
27.
go back to reference Marwick, T. H. (2006). Measurement of strain and strain rate by echocardiography: Ready for prime time? Journal of the American College of Cardiology, 47, 1313–1327.CrossRefPubMed Marwick, T. H. (2006). Measurement of strain and strain rate by echocardiography: Ready for prime time? Journal of the American College of Cardiology, 47, 1313–1327.CrossRefPubMed
28.
go back to reference Lee, A. P., Zhang, Q., Yip, G., Fang, F., Liang, Y. J., Xie, J. M., et al. (2011). LV mechanical dyssynchrony in heart failure with preserved ejection fraction complicating acute coronary syndrome. JACC Cardiovascular Imaging, 4, 348–357.CrossRefPubMed Lee, A. P., Zhang, Q., Yip, G., Fang, F., Liang, Y. J., Xie, J. M., et al. (2011). LV mechanical dyssynchrony in heart failure with preserved ejection fraction complicating acute coronary syndrome. JACC Cardiovascular Imaging, 4, 348–357.CrossRefPubMed
29.
go back to reference Perez, C. M., Hazari, M. S., & Farraj, A. K. (2015). Role of autonomic reflex arcs in cardiovascular responses to air pollution exposure. Cardiovascular Toxicology, 15, 69–78.CrossRefPubMedPubMedCentral Perez, C. M., Hazari, M. S., & Farraj, A. K. (2015). Role of autonomic reflex arcs in cardiovascular responses to air pollution exposure. Cardiovascular Toxicology, 15, 69–78.CrossRefPubMedPubMedCentral
30.
go back to reference Ghilarducci, D. P., & Tjeerdema, R. S. (1995). Fate and effects of acrolein. Reviews of Environmental Contamination and Toxicology, 144, 95–146.PubMed Ghilarducci, D. P., & Tjeerdema, R. S. (1995). Fate and effects of acrolein. Reviews of Environmental Contamination and Toxicology, 144, 95–146.PubMed
31.
go back to reference Moretto, N., Volpi, G., Pastore, F., & Facchinetti, F. (2012). Acrolein effects in pulmonary cells: Relevance to chronic obstructive pulmonary disease. Annals of the New York Academy of Sciences, 1259, 39–46.CrossRefPubMed Moretto, N., Volpi, G., Pastore, F., & Facchinetti, F. (2012). Acrolein effects in pulmonary cells: Relevance to chronic obstructive pulmonary disease. Annals of the New York Academy of Sciences, 1259, 39–46.CrossRefPubMed
32.
go back to reference Pagel, P. S., Nijhawan, N., & Warltier, D. C. (1993). Quantitation of volatile anesthetic-induced depression of myocardial contractility using a single beat index derived from maximal ventricular power. Journal of Cardiothoracic and Vascular Anesthesia, 7, 688–695.CrossRefPubMed Pagel, P. S., Nijhawan, N., & Warltier, D. C. (1993). Quantitation of volatile anesthetic-induced depression of myocardial contractility using a single beat index derived from maximal ventricular power. Journal of Cardiothoracic and Vascular Anesthesia, 7, 688–695.CrossRefPubMed
33.
go back to reference Hatakeyama, N., Ito, Y., & Momose, Y. (1993). Effects of sevoflurane, isoflurane, and halothane on mechanical and electrophysiologic properties of canine myocardium. Anesthesia and Analgesia, 76, 1327–1332.CrossRefPubMed Hatakeyama, N., Ito, Y., & Momose, Y. (1993). Effects of sevoflurane, isoflurane, and halothane on mechanical and electrophysiologic properties of canine myocardium. Anesthesia and Analgesia, 76, 1327–1332.CrossRefPubMed
34.
go back to reference Palmisano, B. W., Mehner, R. W., Stowe, D. F., Bosnjak, Z. J., & Kampine, J. P. (1994). Direct myocardial effects of halothane and isoflurane. Comparison between adult and infant rabbits. Anesthesiology, 81, 718–729.CrossRefPubMed Palmisano, B. W., Mehner, R. W., Stowe, D. F., Bosnjak, Z. J., & Kampine, J. P. (1994). Direct myocardial effects of halothane and isoflurane. Comparison between adult and infant rabbits. Anesthesiology, 81, 718–729.CrossRefPubMed
35.
go back to reference Lairez, O., Lonjaret, L., Ruiz, S., Marchal, P., Franchitto, N., Calise, D., et al. (2013). Anesthetic regimen for cardiac function evaluation by echocardiography in mice: Comparison between ketamine, etomidate and isoflurane versus conscious state. Laboratory Animals, 47, 284–290.CrossRefPubMed Lairez, O., Lonjaret, L., Ruiz, S., Marchal, P., Franchitto, N., Calise, D., et al. (2013). Anesthetic regimen for cardiac function evaluation by echocardiography in mice: Comparison between ketamine, etomidate and isoflurane versus conscious state. Laboratory Animals, 47, 284–290.CrossRefPubMed
36.
go back to reference Lynch, P. J., & Jaffe, C. C. (2006). Heart normal short axis section. New Haven, CT: Creative Commons. Lynch, P. J., & Jaffe, C. C. (2006). Heart normal short axis section. New Haven, CT: Creative Commons.
37.
go back to reference Lynch, P. J., & Jaffe, C. C. (2006). Heart apical 4c anatomy. New Haven, CT: Creative Commons. Lynch, P. J., & Jaffe, C. C. (2006). Heart apical 4c anatomy. New Haven, CT: Creative Commons.
Metadata
Title
Acrolein Inhalation Alters Myocardial Synchrony and Performance at and Below Exposure Concentrations that Cause Ventilatory Responses
Authors
Leslie C. Thompson
Allen D. Ledbetter
Najwa Haykal-Coates
Wayne E. Cascio
Mehdi S. Hazari
Aimen K. Farraj
Publication date
01-04-2017
Publisher
Springer US
Published in
Cardiovascular Toxicology / Issue 2/2017
Print ISSN: 1530-7905
Electronic ISSN: 1559-0259
DOI
https://doi.org/10.1007/s12012-016-9360-4

Other articles of this Issue 2/2017

Cardiovascular Toxicology 2/2017 Go to the issue