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Impact of Acute Pulmonary Embolization on Arterial Stiffening and Right Ventricular Function in Dogs

Abstract

Pulmonary hypertension (PH) can impact right ventricular (RV) function and alter pulmonary artery (PA) stiffness. The response of the RV to an acute increase in pulmonary pressure is unclear. In addition, the relation between total pulmonary arterial compliance and local PA stiffness has not been investigated. We used a combination of right heart catheterization (RHC) and magnetic resonance imaging (MRI) to assess PA stiffening and RV function in dogs before and after acute embolization. We hypothesized that in moderate, acute PH the RV is able to compensate for increased afterload, maintaining adequate coupling. Also, we hypothesized that in the absence of PA remodeling the relative area change in the proximal PA (RAC, a noninvasive index of local area strain) correlates with the total arterial compliance (stroke volume-to-pulse pressure ratio). Our results indicate that, after embolization, RV function is able to accommodate the demand for increased stroke work without uncoupling, albeit at the expense of a reduction of efficiency. In this acute model, RAC showed excellent correlation with total arterial compliance. We used this correlation to assess PA pulse pressure (PP) from noninvasive MRI measurements of stroke volume and RAC. We demonstrated that in acute pulmonary embolism MRI estimates of PP are remarkably close to measurements from RHC. These results, if confirmed in chronic PH and clinically, suggest that monitoring of PH progression by noninvasive methods may be possible.

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References

  1. Asanoi, H., S. Sasayama, and T. Kameyama. Ventriculoarterial coupling in normal and failing heart in humans. Circ. Res. 65(2):483–493, 1989.

    PubMed  Article  CAS  Google Scholar 

  2. Badano, L. P., C. Ginghina, J. Easaw, D. Muraru, M. T. Grillo, P. Lancellotti, B. Pinamonti, G. Coghlan, M. P. Marra, B. A. Popescu, and S. De Vita. Right ventricle in pulmonary arterial hypertension: haemodynamics, structural changes, imaging, and proposal of a study protocol aimed to assess remodelling and treatment effects. Eur. J. Echocardiogr. 11(1):27–37, 2010.

    PubMed  Article  Google Scholar 

  3. Barst, R. J., M. McGoon, A. Torbicki, O. Sitbon, M. J. Krowka, H. Olschewski, and S. Gaine. Diagnosis and differential assessment of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 43(12 Suppl S):40S–47S, 2004.

    PubMed  Article  Google Scholar 

  4. Benetos, A., M. Safar, A. Rudnichi, H. Smulyan, J. Richard, P. Ducimetière, and L. Guize. Pulse pressure: a predictor of long-term cardiovascular mortality in a French male population. Hypertension 30(6):1410–1415, 1997.

    PubMed  Article  CAS  Google Scholar 

  5. Blyth, K. G., R. Syyed, J. Chalmers, J. E. Foster, T. Saba, R. Naeije, C. Melot, and A. J. Peacock. Pulmonary arterial pulse pressure and mortality in pulmonary arterial hypertension. Respir. Med. 101(12):2495–2501, 2007.

    PubMed  Article  Google Scholar 

  6. Brimioulle, S., P. Wauthy, P. Ewalenko, B. Rondelet, F. Vermeulen, F. Kerbaul, and R. Naeije. Single-beat estimation of right ventricular end-systolic pressure–volume relationship. Am. J. Physiol. Heart Circ. Physiol. 284(5):H1625–H1630, 2003.

    PubMed  CAS  Google Scholar 

  7. Brimioulle, S., P. Wauthy, and R. Naeije. Single-Beat evaluation of right ventricular contractility. Crit. Care Med. 33(4):917–918, 2005.

    PubMed  Article  Google Scholar 

  8. Bristow, M. R., L. S. Zisman, B. D. Lowes, W. T. Abraham, D. B. Badesch, B. M. Groves, N. F. Voelkel, D. M. Lynch, and R. A. Quaife. The pressure-overloaded right ventricle in pulmonary hypertension. Chest 114(1 Supplement):101S–106S, 1998.

    PubMed  Article  CAS  Google Scholar 

  9. Brown, K. A., and R. V. Ditchey. Human right ventricular end-systolic pressure–volume relation defined by maximal elastance. Circulation 78(1):81–91, 1988.

    PubMed  Article  CAS  Google Scholar 

  10. Burkhoff, D., and K. Sagawa. Ventricular efficiency predicted by an analytical model. Am. J. Physiol. 250(6):R1021–R1027, 1986.

    PubMed  CAS  Google Scholar 

  11. Champion, H. C., E. D. Michelakis, and P. M. Hassoun. Comprehensive invasive and noninvasive approach to the right ventricle-pulmonary circulation unit. Circulation 120(11):992–1007, 2009.

    PubMed  Article  Google Scholar 

  12. Chantler, P. D., E. G. Lakatta, and S. S. Najjar. Arterial-ventricular coupling: mechanistic insights into cardiovascular performance at rest and during exercise. J. Appl. Physiol. 105(4):1342–1351, 2008.

    PubMed  Article  Google Scholar 

  13. Chin, K. M., N. H. S. Kim, and L. J. Rubin. The right ventricle in pulmonary hypertension. Coron. Artery Dis. 16(1):13–18, 2005.

    PubMed  Article  Google Scholar 

  14. D’Alonzo, G. E., R. J. Barst, S. M. Ayres, E. H. Bergofsky, B. H. Brundage, K. M. Detre, A. P. Fishman, R. M. Goldring, B. M. Groves, and J. T. Kernis. Survival in patients with primary pulmonary hypertension. Results from a national prospective registry. Ann. Intern. Med. 115(5):343–349, 1991.

    PubMed  Google Scholar 

  15. Das, A., R. K. Banerjee, and W. M. Gottliebson. Right ventricular inefficiency in repaired tetralogy of fallot: proof of concept for energy calculations from cardiac MRI data. Ann. Biomed. Eng. 38(12):3674–3687, 2010.

    PubMed  Article  Google Scholar 

  16. Fourie, P. R., A. R. Coetzee, and C. T. Bolliger. Pulmonary artery compliance: its role in right ventricular-arterial coupling. Cardiovasc. Res. 26(9):839–844, 1992.

    PubMed  Article  CAS  Google Scholar 

  17. Gan, C. T., J. Lankhaar, N. Westerhof, J. T. Marcus, A. Becker, J. W. R. Twisk, A. Boonstra, P. E. Postmus, and A. Vonk-Noordegraaf. Noninvasively assessed pulmonary artery stiffness predicts mortality in pulmonary arterial hypertension. Chest 132(6):1906–1912, 2007.

    PubMed  Article  Google Scholar 

  18. Ghuysen, A., B. Lambermont, P. Kolh, V. Tchana-Sato, D. Magis, P. Gerard, V. Mommens, N. Janssen, T. Desaive, and V. D’Orio. Alteration of right ventricular-pulmonary vascular coupling in a porcine model of progressive pressure overloading. Shock 29(2):197–204, 2008.

    PubMed  Google Scholar 

  19. Gupta, K. B., J. E. Bavaria, M. B. Ratcliffe, L. H. Edmunds, Jr., and D. K. Bogen. Measurement of end-systolic pressure–volume relations by intra-aortic balloon occlusion. Circulation 80(4):1016–1028, 1989.

    PubMed  Article  CAS  Google Scholar 

  20. Hyduk, A., J. B. Croft, C. Ayala, K. Zheng, Z. Zheng, and G. A. Mensah. Pulmonary hypertension surveillance—United States, 1980–2002. MMWR Surveill. Summ. 54(5):1–28, 2005.

    PubMed  Google Scholar 

  21. Kerbaul, F., Y. By, V. Gariboldi, C. Mekkaoui, P. Fesler, F. Collart, S. Brimioulle, Y. Jammes, J. Ruf, and R. Guieu. Acute pulmonary embolism decreases adenosine plasma levels in anesthetized pigs. ISRN Cardiol. 2011:750301, 2011.

    PubMed  Google Scholar 

  22. Kuehne, T., S. Yilmaz, P. Steendijk, P. Moore, M. Groenink, M. Saaed, O. Weber, C. B. Higgins, P. Ewert, E. Fleck, E. Nagel, I. Schulze-Neick, and P. Lange. Magnetic resonance imaging analysis of right ventricular pressure–volume loops. Circulation 110(14):2010–2016, 2004.

    PubMed  Article  Google Scholar 

  23. Lambermont, B., A. Ghuysen, P. Kolh, V. Tchana-Sato, P. Segers, P. Gerard, P. Morimont, D. Magis, J. Dogné, B. Masereel, and V. D’Orio. Effects of endotoxic shock on right ventricular systolic function and mechanical efficiency. Cardiovasc. Res. 59(2):412–418, 2003.

    PubMed  Article  CAS  Google Scholar 

  24. Lambermont, B., P. Segers, A. Ghuysen, V. Tchana-Sato, P. Morimont, J. Dogné, P. Kolh, P. Gerard, and V. D’Orio. Comparison between single-beat and multiple-beat methods for estimation of right ventricular contractility. Crit. Care Med. 32(9):1886–1890, 2004.

    PubMed  Article  Google Scholar 

  25. Mahapatra, S., R. A. Nishimura, P. Sorajja, S. Cha, and M. D. McGoon. Relationship of pulmonary arterial capacitance and mortality in idiopathic pulmonary arterial hypertension. J. Am. Coll. Cardiol. 47(4):799–803, 2006.

    PubMed  Article  Google Scholar 

  26. McLaughlin, V. V., S. L. Archer, D. B. Badesch, R. J. Barst, H. W. Farber, J. R. Lindner, M. A. Mathier, M. D. McGoon, M. H. Park, R. S. Rosenson, L. J. Rubin, V. F. Tapson, J. Varga, R. A. Harrington, J. L. Anderson, E. R. Bates, C. R. Bridges, M. J. Eisenberg, V. A. Ferrari, C. L. Grines, M. A. Hlatky, A. K. Jacobs, S. Kaul, R. C. Lichtenberg, J. R. Lindner, D. J. Moliterno, D. Mukherjee, G. M. Pohost, R. S. Rosenson, R. S. Schofield, S. J. Shubrooks, J. H. Stein, C. M. Tracy, H. H. Weitz, and D. J. Wesley. ACCF/AHA 2009 expert consensus document on pulmonary hypertension: a report of the American college of cardiology foundation task force on expert consensus documents and the American heart association: developed in collaboration with the American college of chest physicians, American thoracic society, inc., and the pulmonary hypertension association. Circulation 119(16):2250–2294, 2009.

    PubMed  Article  Google Scholar 

  27. Morimont, P., B. Lambermont, A. Ghuysen, P. Gerard, P. Kolh, P. Lancellotti, V. Tchana-Sato, T. Desaive, and V. D’Orio. Effective arterial elastance as an index of pulmonary vascular load. Am. J. Physiol. Heart Circ. Physiol. 294(6):H2736–H2742, 2008.

    PubMed  Article  CAS  Google Scholar 

  28. Sagawa, K. The end-systolic pressure-volume relation of the ventricle: definition, modifications and clinical use. Circulation 63((6)):1223–1227, 1981.

    PubMed  Article  CAS  Google Scholar 

  29. Sagawa, K., L. Maughan, H. Suga, and K. Sunagawa. Cardiac Contraction and the Pressure–Volume Relationship. New York: Oxford University Press, p. 480, 1988.

    Google Scholar 

  30. Sanz, J., A. Garcia-Alvarez, L. Fernandez-Friera, A. Nair, J. G. Mirelis, S. T. Sawit, S. Pinney, and V. Fuster. Right ventriculo-arterial coupling in pulmonary hypertension: a magnetic resonance study. Heart 98(3):238–243, 2012.

    PubMed  Article  Google Scholar 

  31. Segers, P., S. Brimioulle, N. Stergiopulos, N. Westerhof, R. Naeije, M. Maggiorini, and P. Verdonck. Pulmonary arterial compliance in dogs and pigs: the three-element windkessel model revisited. Am. J. Physiol. 277(2):H725–H731, 1999.

    PubMed  CAS  Google Scholar 

  32. Syyed, R., J. T. Reeves, D. Welsh, D. Raeside, M. K. Johnson, and A. J. Peacock. The relationship between the components of pulmonary artery pressure remains constant under all conditions in both health and disease. Chest 133(3):633–639, 2008.

    PubMed  Article  Google Scholar 

  33. Wauthy, P., A. Pagnamenta, F. Vassalli, R. Naeije, and S. Brimioulle. Right ventricular adaptation to pulmonary hypertension: an interspecies comparison. Am. J. Physiol. Heart Circ. Physiol. 286(4):H1441–H1447, 2004.

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge funding support from NIH 1R01HL105598 (NCC) and Department of Radiology (CJF).

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Correspondence to Naomi C. Chesler.

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Associate Editor Ender A. Finol oversaw the review of this article.

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Bellofiore, A., Roldán-Alzate, A., Besse, M. et al. Impact of Acute Pulmonary Embolization on Arterial Stiffening and Right Ventricular Function in Dogs. Ann Biomed Eng 41, 195–204 (2013). https://doi.org/10.1007/s10439-012-0635-z

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  • DOI: https://doi.org/10.1007/s10439-012-0635-z

Keywords

  • Pulmonary arterial hypertension
  • PAH
  • Ventricular–vascular hemodynamic coupling
  • Cardiac Magnetic Resonance Imaging
  • Pulse pressure