The acute chest syndrome in sickle cell disease: Possible role of nitric oxide in its pathophysiology and treatment

American Journal of Respiratory and Critical Care Medicine

Volumn 159, Issue 5 I, 1999, Pages 1368-1376

  Gladwin, Mark T ^a,b   Schechter, Alan N ^a   Shelhamer, James H ^a   Ognibene, Frederick P ^a,b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOGLOBIN; NITRIC OXIDE;

CLINICAL FEATURE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; GENETIC ANALYSIS; HUMAN; HYPOXIC LUNG VASOCONSTRICTION; INHALATIONAL DRUG ADMINISTRATION; LUNG DISEASE; MICROCIRCULATION; MODEL; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SICKLE CELL ANEMIA;

EID: 0032936879     PISSN: 1073449X     EISSN: None     Source Type: Journal    
DOI: 10.1164/ajrccm.159.5.9810094     Document Type: Review

References (87)

1. Platt, O. S., D. J. Brambilla, W. F. Rosse, P. F. Milner, O. Castro, M. H. Steinberg, and P. P. Klug. 1994, Mortality in sickle cell disease: life expectancy and risk factors for early death. N. Engl. J. Med. 330:1639-1644.
2. Bunn, H. F. 1997. Pathogenesis and treatment of sickle cell disease. N. Engl. J. Med. 337:762-769.
3. Noguchi, C. T., A. N. Schechter, and G. P. Rodgers. 1993. Sickle cell disease pathophysiology. In D. R. Higgs and D. J. Weatherall, editors. Bailliere's Clinical Haematology: The Haemoglobinopathies, Vol. 6/1. Bailliere Tindall, London. 57-91.
4. Phelan, M., S. P. Perrine, M. Brauer, and D. V. Faller. 1995. Sickle erythrocytes, after sickling, regulate the expression of the endothelin-1 gene and protein in human endothelial cells in culture. J. Clin. Invest. 96:1145-1151.
5. Hammerman, S. I., S. Kourembanas, T. J. Conca, M. Tucci, M. Brauer, and H. W. Farber. 1997. Endothelin-1 production during the acute chest syndrome in sickle cell disease. Am. J. Respir. Crit. Care Med. 156:280-285.
6. Stockman, J. A., M. A. Nigro, M. M. Mishkin, and F. A. Oski. 1972. Occlusion of large cerebral vessels in sickle-cell anemia. N. Engl. J. Med. 287:846-849.
7. Rothman, S. M., K. H. Fulling, and J. S. Nelson. 1986. Sickle cell anemia and central nervous system infarction: a neuropathological study. Ann. Neurol. 20:684-690.
8. Adams, R. J., V. C. McKie, L. Hsu, B. Files, E. Vichinsky, C. Pegelow, M. Abboud, D. Gallagher, A. Kutlar, F. T. Nichols, D. R. Bonds, and D. Brambilla. 1998. Prevention of a first stroke by transfusions in children with sickle cell anemia and abnormal results on transcranial doppler ultrasonography. N. Engl. J. Med. 339:5-11.
9. Thomas, A. N., C. Pattison, and G. R. Serjeant. 1982. Causes of death in sickle-cell disease in Jamaica. Br. Med. J. 285:633-635.
10. Lisbona, R., V. Derbekyan, and J. A. Novales-Diaz. 1997. Scintigraphic evidence of pulmonary vascular occlusion in sickle cell disease. J. Nucl. Med. 38:1151-1153.
11. Vichinsky, E. P., L. A. Styles, L. H. Colangelo, E. C. Wright, O. Castro, and B. Nickerson. 1997. Acute chest syndrome in sickle cell disease: clinical presentation and course. Blood 89:1787-1792.
12. Key, N. S., A. Slungaard, L. Dandelet, S. C. Nelson, C. Moertel, L. A. Styles, F. A. Kuypers, and R. R. Bach. 1998. Whole blood tissue factor procoagulant activity is elevated in patients with sickle cell disease. Blood 91:4216-4223.
13. Hebbel, R. P., and G. M. Vercellotti. 1997. The endothelial biology of sickle cell disease. J. Lab. Clin. Med. 129:288-293.
14. Natarajan, M., M. M. Udden, and L. V. McIntire. 1996. Adhesion of sickle red blood cells and damage to interleukin-1β stimulated endothelial cells under flow in vitro. Blood 87:4845-4852.
15. Kumar, A., J. R. Eckmann, R. A. Swerlick, and T. M. Wick. 1996. Phorbol ester stimulation increases sickle erythrocyte adherence to endothelium: a novel pathway involving α4β1 integrin receptors on sickle reticulocytes and fibronectin. Blood 88:4348-4358.
16. Swerlick, R. A., J. R. Eckmann, A. Kumar, M. Jeitler, and T. M. Whick, 1993. α4β1-integrin expression on sickle reticulocytes: vascular cell adhesion molecule-1-dependent binding to endothelium. Blood 82:1891-1899.
17. Gee, B. E., and O. S. Platt. 1995. Sickle erythrocytes adhere to VCAM-1. Blood 85:268-274.
18. Sugihara, K., T. Sugihara, N. Mohandas, and R. P. Hebbel. 1992. Thrombospondin mediates adherence of CD36+ sickle reticulocytes to endothelial cells. Blood 80:2634-2642.
19. Brittain, H. A., J. R. Eckman, R. A. Swerlick, R. J. Howard, and T. M. Wick. 1993. Thrombospondin from activated platelets promotes sickle erythrocyte adherence to human microvascular endothelium under physiologic flow: a potential role for platelet activation in sickle cell vaso-occlusion. Blood 81:2137-2143.
20. Solovey, A., Y. Lin, P. Browne, S. Choong, E. Wayner, and R. P. Hebbel. 1997. Circulating activated endothelial cells in sickle cell anemia. N. Engl. J. Med. 337:1584-1590.
21. Rodgers, G, P., A. N. Schechter, C. T. Noguchi, H. G. Klein, A. W. Nienhuis, and R. F. Bonner. 1984. Periodic microcirculatory flow in patients with sickle-cell disease. N. Engl. J. Med. 311:1534-1538.
22. Rodgers, G. P., A. N. Schechter, C. T. Noguchi, H. G. Klein, A. W. Nienhuis, and R. F. Bonner. 1990. Microcirculator adaptations in sickle cell anemia: reactive hyperemia response. Am. J. Physiol. 258:H113-H120.
23. Norris, S. L., J. R. Gober, L. J. Haywood, J. Halls, W. Boswell, P. Colletti, and M. Terk. 1993. Altered muscle metabolism shown by magnetic resonance spectroscopy in sickle cell disease with leg ulcers. Magn. Reson. Imaging 11:119-123.
24. Hui, K., G. K. Lee, F. Zhang, K. Li, L. Cheung, and W. C. Lincaweaver. 1996. Magnetic resonance imaging detection of vascular occlusion of a pedicled muscle flap. Microsurgery 17:306-312.
25. Fowler, M. D., T. W. Ryschon, R. E. Wysong, C. A. Combs, and R. S. Balaban. 1997. Normalized metabolic stress for 31P-MR spectroscopy studies of human skeletal muscle: MVC vs. muscle volume. J. Appl. Physiol. 83:875-883.
26. Saad, S. T. O., and M. A. Zago. 1991. Leg ulceration and abnormalities of calf blood flow in sickle-cell anemia. Eur, J. Haematol. 46:188-190.
27. Castro, O., D. J. Brambilla, B. Thorington, C. A. Reindorf, R. B. Scott, P. Gillette, J. C. Vera, and P. S. Levy. 1994. The acute chest syndrome in sickle cell disease: incidence and risk factors. Blood 84:643-649.
28. Rucknagel, D. L., K. A. Kalinyak, and M. J. Gelfand. 1991. Rib infarets and acute chest syndrome in sickle cell diseases. Lancet 337:831-833.
29. Cockshott, W. P. 1992. Rib infarcts in sickling disease. Eur. J. Radiol. 14:63-66.
30. Bellet, P. S., K. A. Kalinyak, R. Shukla, M. J. Gelfand, and D. L. Rucknagel. 1995. Incentive spirometry to prevent acute pulmonary complications in sickle cell diseases. N. Engl. J. Med. 333:699-703.
31. Ballas, S. K., and C. H. Park. 1991. Severe hypoxemia secondary to acute sternal infarction in sickle cell anemia. J. Nucl. Med. 32:1617-1618.
32. Weil, J. V., O. Castro, A. B. Malik, G. Rodgers, D. R. Bonds, and T. P. Jacobs. 1993. NHLBI workshop summary: pathogenesis of lung disease in sickle hemoglobinopathies. Am. Rev. Respir. Dis. 148:249-256.
33. Vichinsky, E., and L. Styles. 1996. Sickle cell disease. Pulmonary complications. Hematol. Oncol. Clin. North Am. 10:1275-1287.
34. Godeau, B., A. Schacffer, D. Bachir, J. Fleury-Feith, F. Galacteros, F. Verra, E. Escudier, J. N. Vaillant, C. Brun-Buisson, A. Rahmouni, A. S. Allaoui, and F. Lebargy. 1996. Bronchoalveolar lavage in adult sickle cell patients with acute chest syndrome: value for diagnostic assessment of fat embolism. Am. J. Respir. Crit. Care Med. 153:1691-1696.
35. Vichinsky, E., R. Williams, M. Das, A. N. Earles, N. Lewis, A. Adler, and J. McQuitty. 1994. Pulmonary fat embolism: a distinct cause of severe acute chest syndrome in sickle cell anemia. Blood 83:3107-3112.
36. 2 levels in acute chest syndrome of sickle cell disease. Blood 87:2573-2578.
37. Kirkpatrick, M. B., J. Haynes, and J. B. Bass. 1991. Results of bronchoscopically obtained lower airway cultures from adult sickle cell disease patients with the acute chest syndrome. Am. J. Med. 90:206-210.
38. Miller, S. T., M. R, Hammerschlag, K. Chirgwin, S. P. Rao, P. Roblin, M. Gelling, T. Stilerman, J. Schachter, and G. Cassell. 1991. Role of Chlamydia pneumoniae in acute chest syndrome of sickle cell disease. J. Pediatr. 118:30-33.
39. Aldrich, T. K., S. K. Dhuper, N. S. Patwa, E. Makolo, S. M. Suzuka, S. A. Najeebi, S. Santhanakrishnan, R. L. Nagel, and M. E. Fabry, 1996. Pulmonary entrapment of sickle cells: the role of regional alveolar hypoxia. J. Appl. Physiol. 80:531-539.
40. Scully, R. E., E. J. Mark, W. F. McNecly, S. H. Ebeling, and L. D. Phillips. 1997. Case records of the Massachusetts general hospital: case 34-1997. N. Engl. J. Med. 337:1293-1301.
41. Jia, L., C. Bonaventura, J. Bonaventura, and J. S. Stamler, 1996. S-nitrosohemoglobin: a dynamic activity of blood involved in vascular control. Nature 380:221-226.
42. Stamler, J. S., L. Jia, J. P. Eu, T. J. McMahon, I. T. Demchenko, J. Bonaventura, K. Gernert, and C. A. Piantadosi. 1997. Blood flow regulation by S-nitrosohemoglobin in the physiologic oxygen gradient. Science 276:2034-2037.
43. Gow, A. J., and J. S. Stamler. 1998. Reactions between nitric oxide and haemoglobin under physiological conditions. Nature 391:169-173.
44. Head, C. A., C. Brugnara, R. Martinez-Ruiz, R. M. Kacmarek, K. R. Bridges, D. Kuter, K. D. Bloch, and W. M. Zapol. 1997. Low concentrations of nitric oxide increase oxygen affinity of sickle erythrocytes in vitro and vivo. J. Clin. Invest. 100:1193-1198.
45. Schechter, A. N. 1997. NO therapy? J. Clin. Invest. 100:955-956.
46. Garel, M. C, C. Domenget, F. Galacteros, J. Martin-Caburi, and Y. Beuzard. 1984. Inhibition of erythrocyte sickling by thiol reagents. Mol. Pharmacol. 26:559-565.
47. Garel, M. C., C. Domenget, J. Caburi-Martin, C. Prehu, F. Galacteros, and Y. Beuzard. 1986. Covalent binding of glutathione to hemoglobin: I. Inhibition of hemoglobin S polymerization. J. Biol. Chem. 261:14704-14709.
48. Lopez, B. L., J. Barnett, S. K. Ballas, T. A. Christopher, L. Davis-Moon, and X. Ma. 1996. Nitric oxide metabolite levels in acute vaso-occlusive sickle-cell crisis. Acad. Emerg. Med. 3:1098-1103.
49. French, J. A., 2nd, D. Kenny, J. P. Scott, R. G. Hoffmann, J. D. Wood, A. G. Hudetz, and C. A. Hillery. 1997. Mechanism of stroke in sickle cell disease: sickle erythrocytes decrease cerebral blood flow in rats after nitric oxide synthase inhibition. Blood 89:4591-4599.
50. Pacelli, R., J. Taira, J. A. Cook, D. A. Wink, and M. C. Krishna. 1996. Hydroxyurea reacts with heme proteins to generate nitric oxide. Lancet 347:900.
51. McDade, W. A., H. M. Shaba, N. Boler, and S. Mathics. 1997. Nitric oxide increases the solubility of deoxyhemoglobin S solutions and promotes unsickling of sickled cells. Abstract presented at Annual Meeting of the Natural Sickle Cell Center, Washington DC, September 1997.
52. Moncada, S., and A. Higgs. 1993. The L-arginine-nitric oxide pathway, N. Engl. J. Med. 329:2002-2012.
53. Lancaster, J. R., Jr., 1994. Stimulation of the diffusion and reaction of endogenously produced nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 91: 8137-8141.
54. Lancaster, J. R., Jr. 1997. A tutorial on the diffusibility and reactivity of free nitric oxide. NO: Biol. Chem. 1:18-30.
55. Wink, D. A., I. Hanbauer, M. B. Grisham, F. Laval, R. W. Nims, J. Laval, J. Cook, R. Pacelli, J. Liebmann, M. Krishna, P. C. Ford, and J. B. Mitchell. 1996. Chemical biology of nitric oxide: regulation and protective and toxic mechanisms. Curr. Tup. Cell. Regul. 34:159-187.
56. Deem, S., E. R. Swenson, M. K. Alberts, R. G. Hedges, and M. J. Bishop. 1998. Red-blood-cell augmentation of hypoxic pulmonary vasoconstriction: hematocrit dependence and the importance of nitric oxide. Am. J. Respir. Crit. Care Med. 157:1181-1186.
57. Black, S. M., M. J. Johengen, Z. D. Ma, J. Bristow, and S. J. Soifer. 1997. Ventilation and oxygenation induce endothelial nitric oxide synthase gene expression in the lungs of fetal lambs. J. Clin. Invest. 100:1448-1458.
58. Nelin, L. D., C. J. Thomas, and C. A. Dawson. 1996. Effect of hypoxia on nitric oxide production in neonatal pig lung. Am. J. Physiol. 271: H8-H14.
59. Phelan, M. W., and V. F. Faller. 1996. Hypoxia decreases constitutive nitric oxide synthase transcript and protein in cultured endothelial cells. J. Cell. Physiol. 167:469-476.
60. Johns, R. A., J. M. Linden, and M. J. Peach. 1989. Endotheium-dependent relaxation and cyclic GMP accumulation in rabbit pulmonary artery are selectively impaired by hypoxia. Circ. Res. 65:1508-1515.
61. McQueston, J. A., D. N. Cornfield, I. F. McMurtry, and S. H. Abman. 1993. Effects of oxygen and endogenous L-arginine on EDRF activity in fetal pulmonary circulation. Am. J. Physiol. 264:H865-H871.
62. Cornfield, D. N., H. L. Reeve, S. Tolarova, E. K. Weir, and S. Archer. 1996. Oxygen causes fetal pulmonary vasodilation through activation of a calcium-dependent potassium channel. Proc. Natl. Acad. Sci. U.S.A. 93:8089-8094.
63. Blitzer, M. L., E. Loh, M. A. Roddy, J. S. Stamter, and M. A. Creager. 1996. Endothelium-derived nitric oxide regulates systemic and pulmonary vascular resistance during acute hypoxia in humans. J. Am. Coll. Cardiol. 28:591-596.
64. Gaston, B., J. M. Drazen, J. Loscalzo, and J. S. Stamler. 1994. The biology of nitrogen oxides in the airways. Am. J. Respir. Crit. Care Med. 149:538-551.
65. Guo, F. H., H. R. De Raeve, T. W. Rice, D. J. Stuehr, F. B. Thunnissen, and S. C. Erzurum. 1995. Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc. Natl. Acad. Sci. U.S.A. 92:7809-7813.
66. Janssens, S. P., K. D. Bloch, Z. Nong, R. D. Gerard, P. Zoldhelyi, and D. Collen. 1996. Adenovirus mediated transfer of the human endothelial nitric oxide synthase gene reduces acute hypoxic pulmonary vasconstriction in rats. J. Clin. Invest. 98:317-324.
67. Rairigh, R. L., T. D. Le Cras, D. D. Ivy, J. P. Kinsella, G. Richter, M. P. Horan, I. D. Fan, and S. H. Abman. 1998. Role of inducible nitric oxide synthase in regulation of pulmonary vascular tone in the late gestation ovine fetus. J. Clin. Invest. 101:15-21.
68. Dweik, R. A., D. Laskowski, H. M. Abu-Soud, F. Kaneko, R. Hutte, D. J. Stuehr, and S. C. Erzurum. 1998. Nitric oxide synthesis in the lung: regulation by oxygen through a kinetic mechanism. J. Clin. Invest. 101:660-666.
69. McMurtry, I. F., B. W. Hookway, and S. Roos. 1977. Red blood cells play a crucial role in maintaining vascular reactivity to hypoxia in isolated rat lungs. Chest 71:253-256.
70. McMurtry, I. F., B. W. Hookway, and S. D. Roos. 1978. Red blood cells but not platelets prolong vascular reactivity of isolated rat lungs. Am. J. Physiol. 234:H186-H191.
71. Hakim, T. S., and A. B. Malik. 1988. Hypoxic vasoconstriction in blood and plasma perfused lungs. Respir. Physiol. 72:109-121.
72. Hauge, A. 1968. Conditions governing the pressor response to ventilation hypoxia in isolated perfused rat lungs. Acta Physiol. Scand. 72:33-44.
73. Weissmann, N., F. Grimminger, D. Walmrath, and W. Seeger. 1995. Hypoxic vasoconslriction in buffer-perfused rabbit lungs. Respir. Physiol. 100:159-169.
74. Deem, S. A., M. J. Bishop, and M. K. Alberts. 1995. The effect of anemia on intrapulmonary shunt during atelectasis in rabbits. J. Appl. Physiol. 79:1951-1957.
75. van Agtmael, M. A., J. D. Cheng, and H. C. Nossent. 1994. Acute chest syndrome in adult Afro-Caribbean patients with sickle cell disease: analysis of 81 episodes among 53 patients. Arch. Intern. Med. 154:557-561.
76. Sprinkle, R. H., T. Cole, S. Smith, and G. R. Buchanan. 1986. Acute chest syndrome in children with sickle cell disease. Am. J. Pediatr. Hematol. Oncol. 8:105-110.
77. Wayne, A. S., S. V. Kevy, and D. Nathan. 1993. Transfusion management of sickle cell disease. Blood 81:1109-1123.
78. Mallouh, A. A., and M. Asha. 1988. Beneficial effect of blood transfusion in children with sickle cell chest syndrome. Arch. Pediatr. Adolesc. Med. 142:178-182.
79. Lanzkowsky, P., A. Shende, G. Karayalcin, Y. J. Kim, and A. J. Aballi. 1978. Partial exchange transfusion in sickle cell anemia. Use in children with serious complications. Am. J. Dis. Child. 132:1206-1208.
80. Emre, U., S. T. Miller, M. Gutierez, P. Steiner, S. P. Rao, and M. Rao. 1995. Effect of transfusion in acute chest syndrome of sickle cell disease. J. Pediatr. 127:901-904.
81. Rackoff, W. R., N. Kunkel, J. H. Silber, T. Asakura, and K. OheneFrempong. 1993. Pulse oximetry and factors associated with hemoglobin oxygen desaturation in children with sickle cell disease. Blood 81:3422-3427.
82. Homi, J., L. Levee, D. Higgs, P. Thomas, and G. Serjeant. 1997. Pulse oximetry in a cohort study of sickle cell disease. Clin. Lab. Haematol. 19:17-22.
83. Lonsdorfer, J., P. Bogui, A. Otayeck, E. Bursaux, C. Poyart, and R. Cabannes. 1983. Cardiorespiratory adjustments in chronic sickle cell anemia. Bull. Eur. Physiopathol. Respir. 19:339-344.
84. Bromberg, P. A., and W. N. Jensen. 1967. Arterial oxygen unsaturation in sickle cell disease. Am. Rev. Respir. Dis. 96:400-407.
85. Atz, A. M., and D. L. Wessel. 1997. Inhaled nitric oxide in sickle cell disease with acute chest syndrome. Anesthesiology 87:988-990.
86. Troncy, E., J. P. Collet, S. Shapiro, J. G. Guimond, L. Blair, T. Ducruet, M. Francoeur, M. Charbonneau, and G. Blaise. 1998. Inhaled nitric oxide in acute respiratory distress syndrome: a pilot randomized controlled study. Am. J. Respir. Crit. Care Med. 157:1483-1488.
87. Dellinger, R. P., J. L. Zimmerman, R. W. Taylor, R. C. Straube, D. L. Hauser, G. J. Criner, K. Davis, Jr., T. M. Hyers, and P. Papadakos. 1998. Effects of inhaled nitric oxide in patients with acute respiratory distress syndrome: results of a randomized phase II trial. Inhaled nitric oxide in ARDS study group. Crit. Care Med. 26:15-23.