Echocardiographic markers of elevated pulmonary pressure and left ventricular diastolic dysfunction are associated with exercise intolerance in adults and adolescents with homozygous sickle cell anemia in the United States and United Kingdom

Circulation

Volumn 124, Issue 13, 2011, Pages 1452-1460

  Sachdev, Vandana ^a   Kato, Gregory J ^a   Gibbs, J Simon R ^b   Barst, Robyn J ^c   MacHado, Roberto F ^d   Nouraie, Mehdi ^e   Hassell, Kathryn L ^f   Little, Jane A ^g   Schraufnagel, Dean E ^d   Krishnamurti, Lakshmanan ^h   Novelli, Enrico M ^l   Girgis, Reda E ⁱ   Morris, Claudia R ^j   Rosenzweig, Erika Berman ^c   Badesch, David B ^f   Lanzkron, Sophie ⁱ   Castro, Oswaldo L ^e   Taylor, James G ^a   Hannoush, Hwaida ^a   Goldsmith, Jonathan C ^a   Gladwin, Mark T ^k,l   Gordeuk, Victor R ^e   more..

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^e HOWARD UNIVERSITY   (United States)

^f UNIVERSITY OF COLORADO   (United States)

^g ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^h CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

ⁱ JOHNS HOPKINS UNIVERSITY   (United States)

^j CHILDREN S HOSPITAL OAKLAND   (United States)

^k Department of Medicine   (United States)

^l UNIVERSITY OF PITTSBURGH   (United States)

more..

Author keywords

anemia, sickle cell; diastole; echocardiography; exercise; hypertension, pulmonary

Indexed keywords

ERYTHROPOIETIN; FERRITIN; HEMOGLOBIN S; NITROGEN; SILDENAFIL; UREA;

ADOLESCENT; ADULT; ARTICLE; CARDIOVASCULAR PARAMETERS; CHILD; DIASTOLIC DYSFUNCTION; DISEASE MARKER; ECHOCARDIOGRAPHY; EXERCISE; EXERCISE INTOLERANCE; EXERCISE TEST; EXERCISE TOLERANCE; FEMALE; FERRITIN BLOOD LEVEL; GROUPS BY AGE; HEART LEFT VENTRICLE FAILURE; HEART LEFT VENTRICLE FILLING PRESSURE; HEART LEFT VENTRICLE INFLOW VELOCITY; HEART LEFT VENTRICLE WALL; HEMOLYSIS; HOMOZYGOTE; HORMONE BLOOD LEVEL; HUMAN; LATERAL MITRAL ANNULAR VELOCITY; LUNG ARTERY PRESSURE; MAJOR CLINICAL STUDY; MALE; PREDICTIVE VALUE; PRIORITY JOURNAL; PULMONARY HYPERTENSION; SCHOOL CHILD; SEX DIFFERENCE; SICKLE CELL ANEMIA; SYSTOLIC BLOOD PRESSURE; TISSUE DOPPLER IMAGING; TRICUSPID VALVE REGURGITATION; TRICUSPID VALVE REGURGITATION VELOCITY; UNITED KINGDOM; UNITED STATES; UREA NITROGEN BLOOD LEVEL; WALKING;

ADOLESCENT; ADULT; AGED; ANEMIA, SICKLE CELL; CHILD; ECHOCARDIOGRAPHY; EXERCISE TEST; EXERCISE TOLERANCE; FEMALE; GREAT BRITAIN; HOMOZYGOTE; HUMANS; HYPERTENSION, PULMONARY; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; PREDICTIVE VALUE OF TESTS; PROSPECTIVE STUDIES; PULMONARY ARTERY; TRICUSPID VALVE INSUFFICIENCY; UNITED STATES; VENTRICULAR DYSFUNCTION, LEFT; YOUNG ADULT;

EID: 80053300657     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.032920     Document Type: Article

References (49)

1. Fitzhugh CD, Lauder N, Jonassaint JC, Telen MJ, Zhao X, Wright EC, Gilliam FR, De Castro LM. Cardiopulmonary complications leading to premature deaths in adult patients with sickle cell disease. Am J Hematol. 2010;85:36-40.
2. Sachdev V, Machado RF, Shizukuda Y, Rao YN, Sidenko S, Ernst I, St Peter M, Coles WA, Rosing DR, Blackwelder WC, Castro O, Kato GJ, Gladwin MT. Diastolic dysfunction is an independent risk factor for death in patients with sickle cell disease. J Am Coll Cardiol. 2007;49:472-479. (Pubitemid 46135890)
3. Gladwin MT, Sachdev V, Jison ML, Shizukuda Y, Plehn JF, Minter K, Brown B, Coles WA, Nichols JS, Ernst I, Hunter LA, Blackwelder WC, Schechter AN, Rodgers GP, Castro O, Ognibene FP. Pulmonary hypertension as a risk factor for death in patients with sickle cell disease. N Engl J Med. 2004;350:886-895. (Pubitemid 38252536)
4. Ataga KI, Moore CG, Jones S, Olajide O, Strayhorn D, Hinderliter A, Orringer EP. Pulmonary hypertension in patients with sickle cell disease: a longitudinal study. Br J Haematol. 2006;134:109-115. (Pubitemid 43830036)
5. De Castro LM, Jonassaint JC, Graham FL, Ashley-Koch A, Telen MJ. Pulmonary hypertension associated with sickle cell disease: clinical and laboratory endpoints and disease outcomes. Am J Hematol. 2008;83: 19-25.
6. Castro O, Hoque M, Brown BD. Pulmonary hypertension in sickle cell disease: cardiac catheterization results and survival. Blood. 2003;101: 1257-1261. (Pubitemid 36182493)
7. Collins FS, Orringer EP. Pulmonary hypertension and cor pulmonale in the sickle hemoglobinopathies. Am J Med. 1982;73:814-821. (Pubitemid 13211825)
8. Aessopos A, Farmakis D, Karagiorga M, Voskaridou E, Loutradi A, Hatziliami A, Joussef J, Rombos J, Loukopoulos D. Cardiac involvement in thalassemia intermedia: a multicenter study. Blood. 2001;97: 3411-3416.
9. Heller PG, Grinberg AR, Lencioni M, Molina MM, Roncoroni AJ. Pulmonary hypertension in paroxysmal nocturnal hemoglobinuria. Chest. 1992;102:642-643.
10. Morris CR, Vichinsky EP. Pulmonary hypertension in thalassemia. Ann N Y Acad Sci. 2010;1202:205-213.
11. Morris CR, Kuypers FA, Kato GJ, Lavrisha L, Larkin S, Singer T, Vichinsky EP. Hemolysis-associated pulmonary hypertension in thalassemia. Ann N Y Acad Sci. 2005;1054:481-485. (Pubitemid 43031061)
12. Reiter CD, Wang X, Tanus-Santos JE, Hogg N, Cannon RO 3rd, Schechter AN, Gladwin MT. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat Med. 2002;8:1383-1389. (Pubitemid 36019423)
13. Morris CR, Kato GJ, Poljakovic M, Wang X, Blackwelder WC, Sachdev V, Hazen SL, Vichinsky EP, Morris SM Jr, Gladwin MT. Dysregulated arginine metabolism, hemolysis-associated pulmonary hypertension, and mortality in sickle cell disease. JAMA. 2005;294:81-90. (Pubitemid 41002842)
14. Machado RF, Gladwin MT. Chronic sickle cell lung disease: new insights into the diagnosis, pathogenesis and treatment of pulmonary hypertension. Br J Haematol. 2005;129:449-464. (Pubitemid 40769895)
15. Hsu LL, Champion HC, Campbell-Lee SA, Bivalacqua TJ, Manci EA, Diwan BA, Schimel DM, Cochard AE, Wang X, Schechter AN, Noguchi CT, Gladwin MT. Hemolysis in sickle cell mice causes pulmonary hypertension due to global impairment in nitric oxide bioavailability. Blood. 2007;109:3088-3098. (Pubitemid 46482112)
16. Minniti CP, Sable C, Campbell A, Rana S, Ensing G, Dham N, Onyekwere O, Nouraie M, Kato GJ, Gladwin MT, Castro OL, Gordeuk VR. Elevated tricuspid regurgitant jet velocity in children and adolescents with sickle cell disease: association with hemolysis and hemoglobin oxygen desaturation. Haematologica. 2009;94:340-347.
17. Colombatti R, Maschietto N, Varotto E, Grison A, Grazzina N, Meneghello L, Teso S, Carli M, Milanesi O, Sainati L. Pulmonary hypertension in sickle cell disease children under 10 years of age. Br J Haematol. 2010;150:601-609.
18. Gordeuk VR, Minniti CP, Nouraie M, Campbell AD, Rana SR, Luchtman-Jones L, Sable C, Dham N, Ensing G, Prchal JT, Kato GJ, Gladwin MT, Castro OL. Elevated tricuspid regurgitation velocity and decline in exercise capacity over 22 months of follow up in children and adolescents with sickle cell anemia. Haematologica. 2011;96:33-40.
19. Bunn HF, Nathan DG, Dover GJ, Hebbel RP, Platt OS, Rosse WF, Ware RE. Pulmonary hypertension and nitric oxide depletion in sickle cell disease. Blood. 2010;116:687-692.
20. Gladwin MT, Barst RJ, Castro OL, Gordeuk VR, Hillery CA, Kato GJ, Kim-Shapiro DB, Machado R, Morris CR, Steinberg MH, Vichinsky EP. Pulmonary hypertension and NO in sickle cell. Blood. 2010;116: 852-854.
21. Hebbel RP. Reconstructing sickle cell disease: A data-based analysis of the "hyperhemolysis paradigm" for pulmonary hypertension from the perspective of evidence-based medicine. Am J Hematol. 2011;86: 123-154.
22. Eckman JR, Embury SH. Sickle cell anemia pathophysiology: back to the data. Am J Hematol. 2011;86:121-122.
23. Anthi A, Machado RF, Jison ML, Taveira-Dasilva AM, Rubin LJ, Hunter L, Hunter CJ, Coles W, Nichols J, Avila NA, Sachdev V, Chen CC, Gladwin MT. Hemodynamic and functional assessment of patients with sickle cell disease and pulmonary hypertension. Am J Respir Crit Care Med. 2007;175:1272-1279. (Pubitemid 46905753)
24. Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelista A. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr. 2009;22:107-133.
25. Ommen SR, Nishimura RA, Appleton CP, Miller FA, Oh JK, Redfield MM, Tajik AJ. Clinical utility of Doppler echocardiography and tissue Doppler imaging in the estimation of left ventricular filling pressures: a comparative simultaneous Doppler-catheterization study. Circulation. 2000;102:1788-1794.
26. Skaluba SJ, Litwin SE. Mechanisms of exercise intolerance: insights from tissue Doppler imaging. Circulation. 2004;109:972-977. (Pubitemid 38282849)
27. Grewal J, McCully RB, Kane GC, Lam C, Pellikka PA. Left ventricular function and exercise capacity. JAMA. 2009;301:286-294.
28. Machado RF, Barst RJ, Yovetich NA, Hassell KL, Kato GJ, Gordeuk VR, Gibbs JS, Little JA, Schraufnagel DE, Krishnamurti L, Girgis RE, Morris CR, Berman Rosenzweig E, Badesch DB, Lanzkron S, Onyekwere O, Castro OL, Sachdev V, Waclawiw MA, Woolson R, Goldsmith JC, Gladwin MT. Hospitalization for pain in patients with sickle cell disease treated with sildenafil for elevated TRV and low exercise capacity. Blood. 2011;118:855-864.
29. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ. Recommendations for chamber quantification: a report from the American Society of Echocardiography's Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005;18:1440-1463. (Pubitemid 41821197)
30. Lester SJ, Ryan EW, Schiller NB, Foster E. Best method in clinical practice and in research studies to determine left atrial size. Am J Cardiol. 1999;84:829-832. (Pubitemid 29469795)
31. Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol. 1986;57:450-458. (Pubitemid 16119719)
32. Reesink HJ, van der Plas MN, Verhey NE, van Steenwijk RP, Kloek JJ, Bresser P. Six-minute walk distance as parameter of functional outcome after pulmonary endarterectomy for chronic thromboembolic pulmonary hypertension. J Thorac Cardiovasc Surg. 2007;133:510-516. (Pubitemid 46136286)
33. Buemi M, Senatore M, Gallo GC, Crasci E, Campo S, Sturiale A, Coppolino G, Bolignano D, Frisina N. Pulmonary hypertension and erythropoietin. Kidney Blood Press Res. 2007;30:248-252. (Pubitemid 47076222)
34. Allegra A, Giacobbe MS, Corvaia E, Cinquegrani M, Corvaja E, Giorgianni G, Buemi M. Possible role of erythropoietin in the pathogenesis of chronic cor pulmonale. Nephrol Dial Transplant. 2005;20:2866-2867. (Pubitemid 41672301)
35. Gordeuk VR, Campbell A, Rana S, Nouraie M, Niu X, Minniti CP, Sable C, Darbari D, Dham N, Onyekwere O, Ammosova T, Nekhai S, Kato GJ, Gladwin MT, Castro OL. Relationship of erythropoietin, fetal hemoglobin, and hydroxyurea treatment to tricuspid regurgitation velocity in children with sickle cell disease. Blood. 2009;114:4639-4644.
36. Klings ES, Anton Bland D, Rosenman D, Princeton S, Odhiambo A, Li G, Bernard SA, Steinberg MH, Farber HW. Pulmonary arterial hypertension and left-sided heart disease in sickle cell disease: clinical characteristics and association with soluble adhesion molecule expression. Am J Hematol. 2008;83:547-553. (Pubitemid 351874870)
37. Satoh K, Kagaya Y, Nakano M, Ito Y, Ohta J, Tada H, Karibe A, Minegishi N, Suzuki N, Yamamoto M, Ono M, Watanabe J, Shirato K, Ishii N, Sugamura K, Shimokawa H. Important role of endogenous erythropoietin system in recruitment of endothelial progenitor cells in hypoxia-induced pulmonary hypertension in mice. Circulation. 2006;113: 1442-1450. (Pubitemid 43739441)
38. Ebert BL, Bunn HF. Regulation of the erythropoietin gene. Blood. 1999; 94:1864-1877. (Pubitemid 29430402)
39. Smith TG, Balanos GM, Croft QP, Talbot NP, Dorrington KL, Ratcliffe PJ, Robbins PA. The increase in pulmonary arterial pressure caused by hypoxia depends on iron status. J Physiol. 2008;586(pt 24):5999-6005.
40. Carlini RG, Reyes AA, Rothstein M. Recombinant human erythropoietin stimulates angiogenesis in vitro. Kidney Int. 1995;47:740-745.
41. Bahlmann FH, De Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, Boehm SM, Menne J, Haller H, Fliser D. Erythropoietin regulates endothelial progenitor cells. Blood. 2004;103:921-926. (Pubitemid 38129551)
42. Sundaram N, Tailor A, Mendelsohn L, Wansapura J, Wang X, Higashimoto T, Pauciulo MW, Gottliebson W, Kalra VK, Nichols WC, Kato GJ, Malik P. High levels of placenta growth factor in sickle cell disease promote pulmonary hypertension. Blood. 2010;116:109-112.
43. Srivastava PM, Thomas MC, Calafiore P, MacIsaac RJ, Jerums G, Burrell LM. Diastolic dysfunction is associated with anaemia in patients with type II diabetes. Clin Sci (Lond). 2006;110:109-116. (Pubitemid 43059050)
44. Russo C, Jin Z, Homma S, Rundek T, Elkind MS, Sacco RL, Di Tullio MR. Effect of obesity and overweight on left ventricular diastolic function: a community-based study in an elderly cohort. J Am Coll Cardiol. 2011;57:1368-1374.
45. Kasner M, Westermann D, Steendijk P, Gaub R, Wilkenshoff U, Weitmann K, Hoffmann W, Poller W, Schultheiss HP, Pauschinger M, Tschope C. Utility of Doppler echocardiography and tissue Doppler imaging in the estimation of diastolic function in heart failure with normal ejection fraction: a comparative Doppler-conductance catheterization study. Circulation. 2007;116:637-647. (Pubitemid 47356348)
46. Geske JB, Sorajja P, Nishimura RA, Ommen SR. Evaluation of left ventricular filling pressures by Doppler echocardiography in patients with hypertrophic cardiomyopathy: correlation with direct left atrial pressure measurement at cardiac catheterization. Circulation. 2007;116: 2702-2708. (Pubitemid 350291242)
47. Niu X, Nouraie M, Campbell A, Rana S, Minniti CP, Sable C, Darbari D, Dham N, Reading NS, Prchal JT, Kato GJ, Gladwin MT, Castro OL, Gordeuk VR. Angiogenic and inflammatory markers of cardiopulmonary changes in children and adolescents with sickle cell disease. PLoS One. 2009;4:e7956.
48. Machado RF, Barst RJ, Yovetich NA, Hassell KL, Goldsmith JC, Woolson R, Gordeuk VR, Gibbs S, Little JA, Kato GJ, Schraufnagel DE, Krishnamurti L, Girgis RE, Morris CR, Berman-Rosenzweig E, Badesch DB, Waclawiw MA, Gladwin M. Safety and efficacy of sildenafil therapy for Doppler-defined pulmonary hypertension in patients with sickle cell disease: preliminary results of the Walk-PHaSST clinical trial: ASH Annual Meeting. Blood. 2009;114:571.
49. Ataga KI, Reid M, Ballas SK, Yasin Z, Bigelow C, James LS, Smith WR, Galacteros F, Kutlar A, Hull JH, Stocker JW. Improvements in haemolysis and indicators of erythrocyte survival do not correlate with acute vaso-occlusive crises in patients with sickle cell disease: a phase III randomized, placebo-controlled, double-blind study of the gardos channel blocker senicapoc (ICA-17043). Br J Haematol. 2011;153:92-104.