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.
Similar content being viewed by others
References
Asanoi, H., S. Sasayama, and T. Kameyama. Ventriculoarterial coupling in normal and failing heart in humans. Circ. Res. 65(2):483–493, 1989.
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.
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.
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.
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.
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.
Brimioulle, S., P. Wauthy, and R. Naeije. Single-Beat evaluation of right ventricular contractility. Crit. Care Med. 33(4):917–918, 2005.
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.
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.
Burkhoff, D., and K. Sagawa. Ventricular efficiency predicted by an analytical model. Am. J. Physiol. 250(6):R1021–R1027, 1986.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Sagawa, K. The end-systolic pressure-volume relation of the ventricle: definition, modifications and clinical use. Circulation 63((6)):1223–1227, 1981.
Sagawa, K., L. Maughan, H. Suga, and K. Sunagawa. Cardiac Contraction and the Pressure–Volume Relationship. New York: Oxford University Press, p. 480, 1988.
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.
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.
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.
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.
Acknowledgments
The authors gratefully acknowledge funding support from NIH 1R01HL105598 (NCC) and Department of Radiology (CJF).
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Ender A. Finol oversaw the review of this article.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-012-0635-z