Journal of Cardiovascular Translational Research

, Volume 6, Issue 5, pp 752–761

Myocardial Infarction in Sickle Cell Disease: Use of Translational Imaging to Diagnose an Under-Recognized Problem

  • Paul Chacko
  • Eric H. Kraut
  • Jay Zweier
  • Charles Hitchcock
  • Subha V. Raman
Article

Abstract

Sickle cell disease (SCD) is an inherited disorder in which microvascular occlusion causes complications across multiple organ systems. The precise incidence of myocardial ischemia and infarction (MI), potentially under-recognized microvascular disease-related complications, remains unknown. The absence of typical atherosclerotic lesions seen in other patients with MI suggests a microvascular mechanism of myocardial injury. Cardiac magnetic resonance (CMR) can demonstrate microvascular disease, making it an appealing modality to assess symptomatic SCD patients. We demonstrate in several dramatic instances how CMR is uniquely able to depict cardiac microvascular obstruction in patients with SCD and chest pain, without which the possibility of myocardial injury would almost certainly be otherwise neglected. Much remains unknown regarding ischemic heart disease in patients with SCD including prevalence, detection, and management. Further work to define evaluation and management algorithms for chest pain in SCD and to develop risk assessment tools may reduce sudden cardiac death in this population.

Keywords

Sickle cell disease Myocardial infarction Ischemic heart disease Microcirculation Magnetic resonance 

References

  1. 1.
    Weatherall, D. J. (2010). The inherited diseases of hemoglobin are an emerging global health burden. Blood, 115, 4331–4336.PubMedCrossRefGoogle Scholar
  2. 2.
    NHS Sickle Cell & Thalassaemia Screening Programme. http://sct.screening.nhs.uk/. Accessed 27 April 2012.
  3. 3.
  4. 4.
    Pavlu, J., Ahmed, R. E., O’Regan, D. P., Partridge, J., Lefroy, D. C., & Layton, D. M. (2007). Myocardial infarction in sickle-cell disease. Lancet, 369, 246.PubMedCrossRefGoogle Scholar
  5. 5.
    Powars, D. R., Chan, L. S., Hiti, A., Ramicone, E., & Johnson, C. (2005). Outcome of sickle cell anemia: a 4-decade observational study of 1056 patients. Medicine (Baltimore), 84, 363–376.CrossRefGoogle Scholar
  6. 6.
    Mekontso Dessap, A., Leon, R., Habibi, A., Nzouakou, R., Roudot-Thoraval, F., Adnot, S., Godeau, B., Galacteros, F., Brun-Buisson, C., Brochard, L., & Maitre, B. (2008). Pulmonary hypertension and cor pulmonale during severe acute chest syndrome in sickle cell disease. American Journal of Respiratory and Critical Care Medicine, 177, 646–653.PubMedCrossRefGoogle Scholar
  7. 7.
    Castro, O., & Gladwin, M. T. (2005). Pulmonary hypertension in sickle cell disease: mechanisms, diagnosis, and management. Hematology/Oncology Clinics of North America, 19, 881–896.PubMedCrossRefGoogle Scholar
  8. 8.
    Powars, D., Weidman, J. A., Odom-Maryon, T., Niland, J. C., & Johnson, C. (1988). Sickle cell chronic lung disease: prior morbidity and the risk of pulmonary failure. Medicine (Baltimore), 67, 66–76.Google Scholar
  9. 9.
    Herrick, J. B. (1910). Peculiar elongated and sickled red blood corpuscles in a case of severe anaemia. Archives of Internal Medicine, 6, 517–521.CrossRefGoogle Scholar
  10. 10.
    James, T. N. (2000). Homage to James B. Herrick: a contemporary look at myocardial infarction and at sickle-cell heart disease: the 32nd Annual Herrick Lecture of the Council on Clinical Cardiology of the American Heart Association. Circulation, 101, 1874–1887.PubMedCrossRefGoogle Scholar
  11. 11.
    Fertrin, K. Y., & Costa, F. F. (2010). Genomic polymorphisms in sickle cell disease: implications for clinical diversity and treatment. Expert Review of Hematology, 3, 443–458.PubMedCrossRefGoogle Scholar
  12. 12.
    Stuart, M. J., & Nagel, R. L. (2004). Sickle-cell disease. Lancet, 364, 1343–1360.PubMedCrossRefGoogle Scholar
  13. 13.
    Orkin, S. H., & Higgs, D. R. (2010). Medicine. Sickle cell disease at 100 years. Science, 329, 291–292.PubMedCrossRefGoogle Scholar
  14. 14.
    Lanzkron, S., Strouse, J. J., Wilson, R., Beach, M. C., Haywood, C., Park, H., Witkop, C., Bass, E. B., & Segal, J. B. (2008). Systematic review: Hydroxyurea for the treatment of adults with sickle cell disease. Annals of Internal Medicine, 148, 939–955.PubMedCrossRefGoogle Scholar
  15. 15.
    Morris, C. R. (2008). Mechanisms of vasculopathy in sickle cell disease and thalassemia. Hematology American Society of Hematology Education Program, 2008, 177–185.CrossRefGoogle Scholar
  16. 16.
    Wood, K. C., Hsu, L. L., & Gladwin, M. T. (2008). Sickle cell disease vasculopathy: a state of nitric oxide resistance. Free Radical Biology & Medicine, 44, 1506–1528.CrossRefGoogle Scholar
  17. 17.
    Reiter, C. D., Wang, X., Tanus-Santos, J. E., Hogg, N., Cannon, R. O., 3rd, Schechter, A. N., & Gladwin, M. T. (2002). Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nature Medicine, 8, 1383–1389.PubMedCrossRefGoogle Scholar
  18. 18.
    Aslan, M., & Freeman, B. A. (2004). Oxidant-mediated impairment of nitric oxide signaling in sickle cell disease—mechanisms and consequences. Cellular and Molecular Biology (Noisy-le-Grand, France), 50, 95–105.Google Scholar
  19. 19.
    Machado, R. F., Martyr, S., Kato, G. J., Barst, R. J., Anthi, A., Robinson, M. R., Hunter, L., Coles, W., Nichols, J., Hunter, C., Sachdev, V., Castro, O., & Gladwin, M. T. (2005). Sildenafil therapy in patients with sickle cell disease and pulmonary hypertension. British Journal of Haematology, 130, 445–453.PubMedCrossRefGoogle Scholar
  20. 20.
    Assanasen, C., Quinton, R. A., & Buchanan, G. R. (2003). Acute myocardial infarction in sickle cell anemia. Journal of Pediatric Hematology/Oncology, 25, 978–981.PubMedCrossRefGoogle Scholar
  21. 21.
    Barrett, O., Jr., Saunders, D. E., Jr., McFarland, D. E., & Humphries, J. O. (1984). Myocardial infarction in sickle cell anemia. American Journal of Hematology, 16, 139–147.PubMedCrossRefGoogle Scholar
  22. 22.
    Dang, N. C., Johnson, C., Eslami-Farsani, M., & Haywood, L. J. (2005). Myocardial injury or infarction associated with fat embolism in sickle cell disease: a report of three cases with survival. American Journal of Hematology, 80, 133–136.PubMedCrossRefGoogle Scholar
  23. 23.
    de Montalembert, M., Maunoury, C., Acar, P., Brousse, V., Sidi, D., & Lenoir, G. (2004). Myocardial ischaemia in children with sickle cell disease. Archives of Disease in Childhood, 89, 359–362.PubMedCrossRefGoogle Scholar
  24. 24.
    Deymann, A. J., & Goertz, K. K. (2003). Myocardial infarction and transient ventricular dysfunction in an adolescent with sickle cell disease. Pediatrics, 111, E183–187.PubMedCrossRefGoogle Scholar
  25. 25.
    Martin, C. R., Cobb, C., Tatter, D., Johnson, C., & Haywood, L. J. (1983). Acute myocardial infarction in sickle cell anemia. Archives of Internal Medicine, 143, 830–831.PubMedCrossRefGoogle Scholar
  26. 26.
    Martin, C. R., Johnson, C. S., Cobb, C., Tatter, D., & Haywood, L. J. (1996). Myocardial infarction in sickle cell disease. Journal of the National Medical Association, 88, 428–432.PubMedGoogle Scholar
  27. 27.
    Maunoury, C., Acar, P., de Montalembert, M., & Sidi, D. (2003). Myocardial perfusion in children with sickle cell disease. The American Journal of Cardiology, 91, 374–376.PubMedCrossRefGoogle Scholar
  28. 28.
    McCormick, W. F. (1988). Massive nonatherosclerotic myocardial infarction in sickle cell anemia. The American Journal of Forensic Medicine and Pathology, 9, 151–154.PubMedCrossRefGoogle Scholar
  29. 29.
    Norris, S., Johnson, C. S., & Haywood, L. J. (1991). Sickle cell anemia: does myocardial ischemia occur during crisis? Journal of the National Medical Association, 83, 209–213.PubMedGoogle Scholar
  30. 30.
    Saad, S. T., Arruda, V. R., Junqueira, O. O., Schelini, F. A., & Coelho, O. B. (1990). Acute myocardial infarction in sickle cell anaemia associated with severe hypoxia. Postgraduate Medical Journal, 66, 1068–1070.PubMedCrossRefGoogle Scholar
  31. 31.
    Sherman, S. C., & Sule, H. P. (2004). Acute myocardial infarction in a young man with sickle cell disease. The Journal of Emergency Medicine, 27, 31–35.PubMedCrossRefGoogle Scholar
  32. 32.
    Wang, H., Laslett, L. J., Richman, C. M., & Wun, T. (2004). Acute myocardial infarction in hemoglobin SC disease. Annals of Hematology, 83, 622–624.PubMedGoogle Scholar
  33. 33.
    Oliveira, E. N. G.-P. (1963). Falcemic cardiopathy: report of a case. The American Journal of Cardiology, 11, 686–688.CrossRefGoogle Scholar
  34. 34.
    Manci, E. A., Culberson, D. E., Yang, Y. M., Gardner, T. M., Powell, R., Haynes, J., Jr., Shah, A. K., & Mankad, V. N. (2003). Causes of death in sickle cell disease: an autopsy study. British Journal of Haematology, 123, 359–365.PubMedCrossRefGoogle Scholar
  35. 35.
    Fitzhugh, C. D., Lauder, N., Jonassaint, J. C., Telen, M. J., Zhao, X., Wright, E. C., Gilliam, F. R., & De Castro, L. M. (2010). Cardiopulmonary complications leading to premature deaths in adult patients with sickle cell disease. American Journal of Hematology, 85, 36–40.PubMedGoogle Scholar
  36. 36.
    Platt, O. S., Brambilla, D. J., Rosse, W. F., Milner, P. F., Castro, O., Steinberg, M. H., & Klug, P. P. (1994). Mortality in sickle cell disease. Life expectancy and risk factors for early death. New England Journal of Medicine, 330, 1639–1644.PubMedCrossRefGoogle Scholar
  37. 37.
    Kannel, W. B., Gordon, T., Castelli, W. P., & Margolis, J. R. (1970). Electrocardiographic left ventricular hypertrophy and risk of coronary heart disease. The Framingham study. Annals of Internal Medicine, 72, 813–822.PubMedCrossRefGoogle Scholar
  38. 38.
    Covitz, W., Espeland, M., Gallagher, D., Hellenbrand, W., Leff, S., & Talner, N. (1995). The heart in sickle cell anemia. The Cooperative Study of Sickle Cell Disease (CSSCD). Chest, 108, 1214–1219.PubMedCrossRefGoogle Scholar
  39. 39.
    Lester, L. A., Sodt, P. C., Hutcheon, N., & Arcilla, R. A. (1990). Cardiac abnormalities in children with sickle cell anemia. Chest, 98, 1169–1174.PubMedCrossRefGoogle Scholar
  40. 40.
    Francis, R. B., Jr., & Johnson, C. S. (1991). Vascular occlusion in sickle cell disease: current concepts and unanswered questions. Blood, 77, 1405–1414.PubMedGoogle Scholar
  41. 41.
    Maisel, A., Friedman, H., Flint, L., Koshy, M., & Prabhu, R. (1983). Continuous electrocardiographic monitoring in patients with sickle-cell anemia during pain crisis. Clinical Cardiology, 6, 339–344.PubMedCrossRefGoogle Scholar
  42. 42.
    Pannu, R., Zhang, J., Andraws, R., Armani, A., Patel, P., & Mancusi-Ungaro, P. (2008). Acute myocardial infarction in sickle cell disease: a systematic review. Critical Pathways in Cardiology, 7, 133–138.PubMedCrossRefGoogle Scholar
  43. 43.
    Mansi, I. A., & Rosner, F. (2002). Myocardial infarction in sickle cell disease. Journal of the National Medical Association, 94, 448–452.PubMedGoogle Scholar
  44. 44.
    Thygesen, K., Alpert, J. S., & White, H. D. (2007). Universal definition of myocardial infarction. Journal of the American College of Cardiology, 50, 2173–2195.PubMedCrossRefGoogle Scholar
  45. 45.
    Aslam, A. K., Rodriguez, C., Aslam, A. F., Vasavada, B. C., & Khan, I. A. (2009). Cardiac troponin I in sickle cell crisis. International Journal of Cardiology, 133, 138–139.PubMedCrossRefGoogle Scholar
  46. 46.
    Lippi, G., De Franceschi, L., Salvagno, G. L., Pavan, C., Montagnana, M., & Guidi, G. C. (2009). Cardiac troponin T during sickle cell crisis. International Journal of Cardiology, 136, 357–358.PubMedCrossRefGoogle Scholar
  47. 47.
    Gladwin, M. T., Sachdev, V., Jison, M. L., Shizukuda, Y., Plehn, J. F., Minter, K., Brown, B., Coles, W. A., Nichols, J. S., Ernst, I., Hunter, L. A., Blackwelder, W. C., Schechter, A. N., Rodgers, G. P., Castro, O., & Ognibene, F. P. (2004). Pulmonary hypertension as a risk factor for death in patients with sickle cell disease. The New England Journal of Medicine, 350, 886–895.PubMedCrossRefGoogle Scholar
  48. 48.
    Simmons, B. E., Santhanam, V., Castaner, A., Rao, K. R., Sachdev, N., & Cooper, R. (1988). Sickle cell heart disease. Two-dimensional echo and Doppler ultrasonographic findings in the hearts of adult patients with sickle cell anemia. Archives of Internal Medicine, 148, 1526–1528.PubMedCrossRefGoogle Scholar
  49. 49.
    Parent, F., Bachir, D., Inamo, J., Lionnet, F., Driss, F., Loko, G., Habibi, A., Bennani, S., Savale, L., Adnot, S., Maitre, B., Yaici, A., Hajji, L., O’Callaghan, D. S., Clerson, P., Girot, R., Galacteros, F., & Simonneau, G. (2011). A hemodynamic study of pulmonary hypertension in sickle cell disease. The New England Journal of Medicine, 365, 44–53.PubMedCrossRefGoogle Scholar
  50. 50.
    Sachdev, V., Machado, R. F., Shizukuda, Y., Rao, Y. N., Sidenko, S., Ernst, I., St Peter, M., Coles, W. A., Rosing, D. R., Blackwelder, W. C., Castro, O., Kato, G. J., & Gladwin, M. T. (2007). Diastolic dysfunction is an independent risk factor for death in patients with sickle cell disease. Journal of the American College of Cardiology, 49, 472–479.PubMedCrossRefGoogle Scholar
  51. 51.
    Peltier, M., Vancraeynest, D., Pasquet, A., Ay, T., Roelants, V., D’Hondt, A. M., Melin, J. A., & Vanoverschelde, J. L. (2004). Assessment of the physiologic significance of coronary disease with dipyridamole real-time myocardial contrast echocardiography. Comparison with technetium-99m sestamibi single-photon emission computed tomography and quantitative coronary angiography. Journal of the American College of Cardiology, 43, 257–264.PubMedCrossRefGoogle Scholar
  52. 52.
    Almeida, A. G., Araujo, F., Rego, F., David, C., Lopes, M. G., & Ducla-Soares, J. (2008). Abnormal myocardial flow reserve in sickle cell disease: a myocardial contrast echocardiography study. Echocardiography, 25, 591–599.PubMedCrossRefGoogle Scholar
  53. 53.
    Honos, G., Amyot, R., Choy, J., Leong-Poi, H., Schnell, G., & Yu, E. (2007). Contrast echocardiography in Canada: Canadian Cardiovascular Society/Canadian Society of Echocardiography position paper. Canadian Journal of Cardiology, 23, 351–356.PubMedCrossRefGoogle Scholar
  54. 54.
    Gerber, B. L., Raman, S. V., Nayak, K., Epstein, F. H., Ferreira, P., Axel, L., & Kraitchman, D. L. (2008). Myocardial first-pass perfusion cardiovascular magnetic resonance: history, theory, and current state of the art. Journal of Cardiovascular Magnetic Resonance, 10, 18.PubMedCrossRefGoogle Scholar
  55. 55.
    Panting, J. R., Gatehouse, P. D., Yang, G. Z., Grothues, F., Firmin, D. N., Collins, P., & Pennell, D. J. (2002). Abnormal subendocardial perfusion in cardiac syndrome X detected by cardiovascular magnetic resonance imaging. The New England Journal of Medicine, 346, 1948–1953.PubMedCrossRefGoogle Scholar
  56. 56.
    Raman, S. V., Simonetti, O. P., Cataland, S. R., & Kraut, E. H. (2006). Myocardial ischemia and right ventricular dysfunction in adult patients with sickle cell disease. Haematologica, 91, 1329–1335.PubMedGoogle Scholar
  57. 57.
    Carpenter JP, He T, Kirk P, Roughton M, Anderson LJ, de Noronha SV, Sheppard MN, Porter JB, Walker JM, Wood JC, Galanello R, Forni G, Catani G, Matta G, Fucharoen S, Fleming A, House MJ, Black G, Firmin DN, St Pierre TG, Pennell DJ (2011) On T2* magnetic resonance and cardiac iron. Circulation 123:1519–1528Google Scholar
  58. 58.
    Wood, J. C., Tyszka, J. M., Carson, S., Nelson, M. D., & Coates, T. D. (2004). Myocardial iron loading in transfusion-dependent thalassemia and sickle cell disease. Blood, 103, 1934–1936.PubMedCrossRefGoogle Scholar
  59. 59.
    Kim, R. J., Fieno, D. S., Parrish, T. B., Harris, K., Chen, E. L., Simonetti, O., Bundy, J., Finn, J. P., Klocke, F. J., & Judd, R. M. (1999). Relationship of MRI delayed contrast enhancement to irreversible injury, infarct age, and contractile function. Circulation, 100, 1992–2002.PubMedCrossRefGoogle Scholar
  60. 60.
    Anderson, J. L., Adams, C. D., Antman, E. M., Bridges, C. R., Califf, R. M., Casey, D. E., Jr., Chavey, W. E., 2nd, Fesmire, F. M., Hochman, J. S., Levin, T. N., Lincoff, A. M., Peterson, E. D., Theroux, P., Wenger, N. K., Wright, R. S., Smith, S. C., Jr., Jacobs, A. K., Halperin, J. L., Hunt, S. A., Krumholz, H. M., Kushner, F. G., Lytle, B. W., Nishimura, R., Ornato, J. P., Page, R. L., & Riegel, B. (2007). ACC/AHA 2007 guidelines for the management of patients with unstable angina/non-ST-elevation myocardial infarction: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 2002 Guidelines for the Management of Patients With Unstable Angina/Non-ST-Elevation Myocardial Infarction) developed in collaboration with the American College of Emergency Physicians, the Society for Cardiovascular Angiography and Interventions, and the Society of Thoracic Surgeons endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation and the Society for Academic Emergency Medicine. Journal of the American College of Cardiology, 50, e1–e157.PubMedCrossRefGoogle Scholar
  61. 61.
    Antman, E. M., Hand, M., Armstrong, P. W., Bates, E. R., Green, L. A., Halasyamani, L. K., Hochman, J. S., Krumholz, H. M., Lamas, G. A., Mullany, C. J., Pearle, D. L., Sloan, M. A., Smith, S. C., Jr., Anbe, D. T., Kushner, F. G., Ornato, J. P., Jacobs, A. K., Adams, C. D., Anderson, J. L., Buller, C. E., Creager, M. A., Ettinger, S. M., Halperin, J. L., Hunt, S. A., Lytle, B. W., Nishimura, R., Page, R. L., Riegel, B., Tarkington, L. G., & Yancy, C. W. (2008). 2007 Focused Update of the ACC/AHA 2004 Guidelines for the Management of Patients With ST-Elevation Myocardial Infarction: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines: developed in collaboration with the Canadian Cardiovascular Society endorsed by the American Academy of Family Physicians: 2007 Writing Group to Review New Evidence and Update the ACC/AHA 2004 Guidelines for the Management of Patients With ST-Elevation Myocardial Infarction, Writing on Behalf of the 2004 Writing Committee. Circulation, 117, 296–329.PubMedCrossRefGoogle Scholar
  62. 62.
    Russell, M. O., Goldberg, H. I., Hodson, A., Kim, H. C., Halus, J., Reivich, M., & Schwartz, E. (1984). Effect of transfusion therapy on arteriographic abnormalities and on recurrence of stroke in sickle cell disease. Blood, 63, 162–169.PubMedGoogle Scholar
  63. 63.
    Khalique Z, Pavlu J, Lefroy D, Layton M (2010) Erythrocytapheresis in the prevention of recurrent myocardial infarction in sickle cell disease. American Journal of Hematology 85:91Google Scholar
  64. 64.
    Atz, A. M., & Wessel, D. L. (1997). Inhaled nitric oxide in sickle cell disease with acute chest syndrome. Anesthesiology, 87, 988–990.PubMedCrossRefGoogle Scholar
  65. 65.
    Sullivan, K. J., Goodwin, S. R., Evangelist, J., Moore, R. D., & Mehta, P. (1999). Nitric oxide successfully used to treat acute chest syndrome of sickle cell disease in a young adolescent. Critical Care Medicine, 27, 2563–2568.PubMedCrossRefGoogle Scholar
  66. 66.
    Head CA, Swerdlow P, McDade WA, Joshi RM, Ikuta T, Cooper ML, Eckman JR (2010) Beneficial effects of nitric oxide breathing in adult patients with sickle cell crisis. American Journal of Hematology 85:800–802Google Scholar
  67. 67.
    Gladwin MT, Kato GJ, Weiner D, Onyekwere OC, Dampier C, Hsu L, Hagar RW, Howard T, Nuss R, Okam MM, Tremonti CK, Berman B, Villella A, Krishnamurti L, Lanzkron S, Castro O, Gordeuk VR, Coles WA, Peters-Lawrence M, Nichols J, Hall MK, Hildesheim M, Blackwelder WC, Baldassarre J, Casella JF (2011) Nitric oxide for inhalation in the acute treatment of sickle cell pain crisis: a randomized controlled trial. JAMA 305:893–902Google Scholar
  68. 68.
    Hataishi, R., Rodrigues, A. C., Neilan, T. G., Morgan, J. G., Buys, E., Shiva, S., Tambouret, R., Jassal, D. S., Raher, M. J., Furutani, E., Ichinose, F., Gladwin, M. T., Rosenzweig, A., Zapol, W. M., Picard, M. H., Bloch, K. D., & Scherrer-Crosbie, M. (2006). Inhaled nitric oxide decreases infarction size and improves left ventricular function in a murine model of myocardial ischemia–reperfusion injury. American Journal of Physiology. Heart and Circulatory Physiology, 291, H379–H384.PubMedCrossRefGoogle Scholar
  69. 69.
    Theuns, D. A., Smith, T., Hunink, M. G., Bardy, G. H., & Jordaens, L. (2010). Effectiveness of prophylactic implantation of cardioverter-defibrillators without cardiac resynchronization therapy in patients with ischaemic or non-ischaemic heart disease: a systematic review and meta-analysis. Europace, 12, 1564–1570.PubMedCrossRefGoogle Scholar
  70. 70.
    Fibach, E. (2001). Cell culture and animal models to screen for promising fetal hemoglobin-stimulating compounds. Seminars in Hematology, 38, 374–381.PubMedCrossRefGoogle Scholar
  71. 71.
    Hebbel, R. P., Vercellotti, G. M., Pace, B. S., Solovey, A. N., Kollander, R., Abanonu, C. F., Nguyen, J., Vineyard, J. V., Belcher, J. D., Abdulla, F., Osifuye, S., Eaton, J. W., Kelm, R. J., Jr., & Slungaard, A. (2010). The HDAC inhibitors trichostatin A and suberoylanilide hydroxamic acid exhibit multiple modalities of benefit for the vascular pathobiology of sickle transgenic mice. Blood, 115, 2483–2490.PubMedCrossRefGoogle Scholar
  72. 72.
    Woodruff, A. W. (1970). Sickle-cell anaemia with complicating coronary infarction. Proceedings of the Royal Society of Medicine, 63, 1314.Google Scholar
  73. 73.
    Rubler, S., & Fleischer, R. A. (1967). Sickle cell states and cardiomyopathy. Sudden death due to pulmonary thrombosis and infarction. The American Journal of Cardiology, 19, 867–873.PubMedCrossRefGoogle Scholar
  74. 74.
    Uzsoy, N. K. (1964). Cardiovascular findings in patients with sickle cell anemia. The American Journal of Cardiology, 13, 320–328.PubMedCrossRefGoogle Scholar
  75. 75.
    Tanner, M. A., Westwood, M. A., & Pennell, D. J. (2006). Myocardial infarction following sickle cell chest syndrome. British Journal of Haematology, 134, 2.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Paul Chacko
    • 1
  • Eric H. Kraut
    • 1
  • Jay Zweier
    • 1
  • Charles Hitchcock
    • 1
  • Subha V. Raman
    • 1
  1. 1.Davis Heart and Lung Research InstituteThe Ohio State UniversityColumbusUSA

Personalised recommendations