Evolution of sickle cell disease from a life-threatening disease of children to a chronic disease of adults: The last 40 years

American Journal of Hematology

Volumn 91, Issue 1, 2016, Pages 5-14

  Chaturvedi, Shruti ^a   Debaun, Michael R ^b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL PRO BRAIN NATRIURETIC PEPTIDE; HEMOGLOBIN F; HYDROXYUREA; PENICILLIN DERIVATIVE; PNEUMOCOCCUS VACCINE; ANTIINFECTIVE AGENT; ANTISICKLING AGENT;

ADULT DISEASE; ANTIBIOTIC PROPHYLAXIS; ARTICLE; ASTHMA; BONE MARROW SUPPRESSION; BRAIN INFARCTION; CEREBROVASCULAR ACCIDENT; CHILDHOOD DISEASE; CHILDHOOD MORTALITY; CHRONIC DISEASE; COR PULMONALE; DELAYED PUBERTY; DISEASE COURSE; DISEASE ERADICATION; ERECTILE DYSFUNCTION; FEVER; HAEMOPHILUS INFLUENZAE TYPE B; HEALTH CARE DISPARITY; HEART MUSCLE ISCHEMIA; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HIGHEST INCOME GROUP; HUMAN; HYPOGONADISM; INFERTILITY; LOWEST INCOME GROUP; MENINGITIS; NEUROIMAGING; NEWBORN SCREENING; NUCLEAR MAGNETIC RESONANCE IMAGING; PARENTING EDUCATION; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PREGNANCY COMPLICATION; PRIAPISM; PRIORITY JOURNAL; PULMONARY HYPERTENSION; QUALITY OF LIFE; RECURRENCE RISK; REPRODUCTIVE HEALTH; SEPSIS; SEPTICEMIA; SICKLE CELL ANEMIA; SILENT CEREBRAL INFARCTION; SOCIOECONOMICS; STREPTOCOCCUS PNEUMONIAE; SURGICAL MORTALITY; TRANSCRANIAL DOPPLER; UNITED STATES; VACCINATION; ADULT; ANEMIA, SICKLE CELL; BLOOD TRANSFUSION; CHILD; COMPLICATION; INFANT; MORTALITY; NEWBORN; PRESCHOOL CHILD; STROKE; TRENDS;

ADULT; ANEMIA, SICKLE CELL; ANTI-BACTERIAL AGENTS; ANTIBIOTIC PROPHYLAXIS; ANTISICKLING AGENTS; BLOOD TRANSFUSION; CHILD; CHILD, PRESCHOOL; CHRONIC DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; HYDROXYUREA; INFANT; INFANT, NEWBORN; MORTALITY; NEONATAL SCREENING; PENICILLINS; STROKE;

EID: 84954242478     PISSN: 03618609     EISSN: 10968652     Source Type: Journal    
DOI: 10.1002/ajh.24235     Document Type: Article

References (144)

1. Scott RB. Reflections on the current status of the national sickle cell disease program in the United States. J Natl Med Assoc 1979;71:679-681.
2. Weatherall DJ. The inherited diseases of hemoglobin are an emerging global health burden. Blood 2010;115:4331-4336.
3. Therrell BL Jr, Lloyd-Puryear MA, Eckman JR, et al. Newborn screening for sickle cell diseases in the United States: A review of data spanning 2 decades. Semin Perinatol 2015;39:238-251.
4. Lorey FW, Arnopp J, Cunningham GC. Distribution of hemoglobinopathy variants by ethnicity in a multiethnic state. Genet Epidemiol 1996;13:501-512.
5. Hassell KL. Population estimates of sickle cell disease in the U.S. Am J Prev Med 2010;38:S512-521.
6. Herrick JB. Peculiar elongated and sickle-shaped red blood corpuscles in a case of severe anemia. Arch Intern Med (Chic) 1910;6:517-521.
7. Pauling L, Itano HA, et al. Sickle cell anemia, a molecular disease. Science 1949;109:443.
8. Beet EA. The genetics of the sickle-cell trait in a Bantu tribe. Ann Eugen 1949;14:279-284.
9. Neel JV. The inheritance of sickle cell anemia. Science 1949;110:64-66.
10. Ingram VM. A specific chemical difference between the globins of normal human and sickle-cell anaemia haemoglobin. Nature 1956;178:792-794.
11. Hunt JA, Ingram VM. Allelomorphism and the chemical differences of the human haemoglobins A, S and C. Nature 1958;181:1062-1063.
12. Bunn HF. Pathogenesis and treatment of sickle cell disease. N Engl J Med 1997;337:762-769.
13. Quinn CT, Rogers ZR, McCavit TL, et al. Improved survival of children and adolescents with sickle cell disease. Blood 2010;115:3447-3452.
14. Platt OS, Brambilla DJ, Rosse WF, et al. Mortality in sickle cell disease. Life expectancy and risk factors for early death. N Engl J Med 1994;330:1639-1644.
15. Lanzkron S, Carroll CP, Haywood C Jr. Mortality rates and age at death from sickle cell disease: U.S., 1979-2005. Public Health Rep 2013;128:110-116.
16. Yanni E, Grosse SD, Yang Q, et al. Trends in pediatric sickle cell disease-related mortality in the United States, 1983-2002. J Pediatr 2009;154:541-545.
17. Lobo CL, Pinto JF, Nascimento EM, et al. The effect of hydroxcarbamide therapy on survival of children with sickle cell disease. Br J Haematol 2013;161:852-860.
18. Scott RB. Health care priority and sickle cell anemia. JAMA 1970;214:731-734.
19. Lee A, Thomas P, Cupidore L, et al. Improved survival in homozygous sickle cell disease: Lessons from a cohort study. BMJ 1995;311:1600-1602.
20. Gill FM, Sleeper LA, Weiner SJ, et al. Clinical events in the first decade in a cohort of infants with sickle cell disease. Cooperative Study of Sickle Cell Disease. Blood 1995;86:776-783.
21. Le PQ, Gulbis B, Dedeken L, et al. Survival among children and adults with sickle cell disease in Belgium: Benefit from hydroxyurea treatment. Pediatric Blood Cancer 2015;62:1956-1961.
22. Elmariah H, Garrett ME, De Castro LM, et al. Factors associated with survival in a contemporary adult sickle cell disease cohort. Am J Hematol 2014;89:530-535.
23. Fitzhugh CD, Lauder N, Jonassaint JC, et al. Cardiopulmonary complications leading to premature deaths in adult patients with sickle cell disease. Am J Hematol 2010;85:36-40.
24. Darbari DS, Kple-Faget P, Kwagyan J, et al. Circumstances of death in adult sickle cell disease patients. Am J Hematol 2006;81:858-863.
25. Powars DR, Chan LS, Hiti A, et al. Outcome of sickle cell anemia: a 4-decade observational study of 1056 patients. Medicine (Baltimore) 2005;84:363-376.
26. Ogun GO, Ebili H, Kotila TR. Autopsy findings and pattern of mortality in Nigerian sickle cell disease patients. Pan Afr Med J 2014;18:30.
27. Owusu-Ansah A, Ihunnah CA, Walker AL, et al. Inflammatory targets of therapy in sickle cell disease. Transl Res 2015 [Epub ahead of print].
28. Overturf GD, Powars D, Baraff LJ. Bacterial meningitis and septicemia in sickle cell disease. Am J Dis Child (1960) 1977;131:784-787.
29. Lobel JS, Bove KE. Clinicopathologic characteristics of septicemia in sickle cell disease. Am J Dis Child 1982;136:543-547.
30. Vichinsky E, Hurst D, Earles A, et al. Newborn screening for sickle cell disease: Effect on mortality. Pediatrics 1988;81:749-755.
31. Zarkowsky HS, Gallagher D, Gill FM, et al. Bacteremia in sickle hemoglobinopathies. J Pediatr 1986;109:579-585.
32. Leikin SL, Gallagher D, Kinney TR, et al. Mortality in children and adolescents with sickle cell disease. Cooperative study of sickle cell disease. Pediatrics 1989;84:500-508.
33. John AB, Ramlal A, Jackson H, et al. Prevention of pneumococcal infection in children with homozygous sickle cell disease. Br Med J (Clin Res Ed) 1984;288:1567-1570.
34. Gaston MH, Verter JI, Woods G, et al. Prophylaxis with oral penicillin in children with sickle cell anemia. A randomized trial. N Engl J Med 1986;314:1593-1599.
35. Barrett-Connor E. Bacterial infection and sickle cell anemia. An analysis of 250 infections in 166 patients and a review of the literature. Medicine (Baltimore) 1971;50:97-112.
36. Robinson MG, Watson RJ. Pneumococcal meningitis in sickle-cell anemia. N Engl J Med 1966;274:1006-1008.
37. Eeckels R, Gatti F, Renoirte AM. Abnormal distribution of haemoglobin genotypes in Negro children with severe bacterial infections. Nature 1967;216:382
38. Powars D, Overturf G, Weiss J, et al. Pneumococcal septicemia in children with sickle cell anemia. Changing trend of survival. JAMA 1981;245:1839-1842.
39. Powars DR. Natural history of sickle cell disease-The first ten years. Semin Hematol 1975;12:267-285.
40. Rogers DW, Vaidya S, Serjeant GR. Early splenomegaly in homozygous sickle-cell disease: An indicator of susceptibility to infection. Lancet 1978;2:963-965.
41. Sanhadji K, Chout R, Gessain A, et al. Cell-mediated immunity in patients with sickle cell anaemia. Thymus 1988;12:203-213.
42. Johnston RB Jr, Newman SL, Struth AG. An abnormality of the alternate pathway of complement activation in sickle-cell disease. N Engl J Med 1973;288:803-808.
43. Winkelstein JA, Drachman RH. Deficiency of pneumococcal serum opsonizing activity in sickle-cell disease. N Engl J Med 1968;279:459-466.
44. Halasa NB, Shankar SM, Talbot TR, et al. Incidence of invasive pneumococcal disease among individuals with sickle cell disease before and after the introduction of the pneumococcal conjugate vaccine. Clin Infect Dis 2007;44:1428-1433.
45. Platt OS, Thorington BD, Brambilla DJ, et al. Pain in sickle cell disease. Rates and risk factors. N Engl J Med 1991;325:11-16.
46. Powars DR, Weiss JN, Chan LS, et al. Is there a threshold level of fetal hemoglobin that ameliorates morbidity in sickle cell anemia? Blood 1984;63:921-926.
47. Platt OS, Orkin SH, Dover G, et al. Hydroxyurea enhances fetal hemoglobin production in sickle cell anemia. J Clin Invest 1984;74:652-656.
48. Rodgers GP, Dover GJ, Noguchi CT, et al. Hematologic responses of patients with sickle cell disease to treatment with hydroxyurea. N Engl J Med 1990;322:1037-1045.
49. Charache S, Dover GJ, Moore RD, et al. Hydroxyurea: effects on hemoglobin F production in patients with sickle cell anemia. Blood 1992;79:2555-2565.
50. Charache S, Terrin ML, Moore RD, et al. Effect of hydroxyurea on the frequency of painful crises in sickle cell anemia. Investigators of the Multicenter Study of Hydroxyurea in Sickle Cell Anemia. N Engl J Med 1995;332:1317-1322.
51. Ballas SK, Barton FB, Waclawiw MA, et al. Hydroxyurea and sickle cell anemia: Effect on quality of life. Health Qual Life Outcomes 2006;4:59
52. Hankins JS, Ware RE, Rogers ZR, et al. Long-term hydroxyurea therapy for infants with sickle cell anemia: The HUSOFT extension study. Blood 2005;106:2269-2275.
53. Thornburg CD, Dixon N, Burgett S, et al. A pilot study of hydroxyurea to prevent chronic organ damage in young children with sickle cell anemia. Pediatr Blood Cancer 2009;52:609-615.
54. Kinney TR, Helms RW, O'Branski EE, et al. Safety of hydroxyurea in children with sickle cell anemia: Results of the HUG-KIDS study, a phase I/II trial. Pediatric Hydroxyurea Group. Blood 1999;94:1550-1554.
55. Wang WC, Ware RE, Miller ST, et al. Hydroxycarbamide in very young children with sickle-cell anaemia: A multicentre, randomised, controlled trial (BABY HUG). Lancet 2011;377:1663-1672.
56. Thompson BW, Miller ST, Rogers ZR, et al. The pediatric hydroxyurea phase III clinical trial (BABY HUG): challenges of study design. Pediatr Blood Cancer 2010;54:250-255.
57. Steinberg MH, Barton F, Castro O, et al. Effect of hydroxyurea on mortality and morbidity in adult sickle cell anemia: Risks and benefits up to 9 years of treatment. JAMA 2003;289:1645-1651.
58. Steinberg MH, McCarthy WF, Castro O, et al. The risks and benefits of long-term use of hydroxyurea in sickle cell anemia: A 17.5 year follow-up. Am J Hematol 2010;85:403-408.
59. Voskaridou E, Christoulas D, Bilalis A, et al. The effect of prolonged administration of hydroxyurea on morbidity and mortality in adult patients with sickle cell syndromes: Results of a 17-year, single-center trial (LaSHS). Blood 2010;115:2354-2363.
60. Enninful-Eghan H, Moore RH, Ichord R, et al. Transcranial Doppler ultrasonography and prophylactic transfusion program is effective in preventing overt stroke in children with sickle cell disease. J Pediatr 2010;157:479-484.
61. Ohene-Frempong K, Weiner SJ, Sleeper LA, et al. Cerebrovascular accidents in sickle cell disease: rates and risk factors. Blood 1998;91:288-294.
62. Powars D, Wilson B, Imbus C, et al. The natural history of stroke in sickle cell disease. Am J Med 1978;65:461-471.
63. Adams RJ, McKie VC, Hsu L, et al. Prevention of a first stroke by transfusions in children with sickle cell anemia and abnormal results on transcranial Doppler ultrasonography. N Engl J Med 1998;339:5-11.
64. Adams RJ, Brambilla D. Discontinuing prophylactic transfusions used to prevent stroke in sickle cell disease. N Engl J Med 2005;353:2769-2778.
65. Ballas SK. Iron overload is a determinant of morbidity and mortality in adult patients with sickle cell disease. Semin Hematol 2001;38:30-36.
66. Gulbis B, Haberman D, Dufour D, et al. Hydroxyurea for sickle cell disease in children and for prevention of cerebrovascular events: The Belgian experience. Blood 2005;105:2685-2690.
67. Kratovil T, Bulas D, Driscoll MC, et al. Hydroxyurea therapy lowers TCD velocities in children with sickle cell disease. Pediatr Blood Cancer 2006;47:894-900.
68. Zimmerman SA, Schultz WH, Burgett S, et al. Hydroxyurea therapy lowers transcranial Doppler flow velocities in children with sickle cell anemia. Blood 2007;110:1043-1047.
69. Lagunju I, Brown BJ, Sodeinde O. Hydroxyurea lowers transcranial Doppler flow velocities in children with sickle cell anaemia in a Nigerian cohort. Pediatr Blood Cancer 2015;62:1587-1591.
70. Galadanci NA, Abdullahi SU, Tabari MA, et al. Primary stroke prevention in Nigerian children with sickle cell disease (SPIN): Challenges of conducting a feasibility trial. Pediatr Blood Cancer 2015;62:395-401.
71. Lefevre N, Dufour D, Gulbis B, et al. Use of hydroxyurea in prevention of stroke in children with sickle cell disease. Blood 2008;111:963-964; author reply 964.
72. Ware RE, Davis BR, Schultz WH, et al. Hydroxycarbamide versus chronic transfusion for maintenance of transcranial doppler flow velocities in children with sickle cell anaemia-TCD With Transfusions Changing to Hydroxyurea (TWiTCH): a multicentre, open-label, phase 3, non-inferiority trial. Lancet 2015 [Epub ahead of print].
73. DeBaun MR, Abdullahi SU, Tabari MA, et al. Acceptability and safety of hydroxyurea for primary prevention of stroke in children with sickle cell disease in Nigeria. Blood 2014;124:4021.
74. Sarnaik S, Soorya D, Kim J, et al. Periodic transfusions for sickle cell anemia and CNS infarction. Am J Dis Child 1979;133:1254-1257.
75. Lusher JM, Haghighat H, Khalifa AS. A prophylactic transfusion program for children with sickle cell anemia complicated by CNS infarction. Am J Hematol 1976;1:265-273.
76. Ware RE, Helms RW. Stroke with transfusions changing to hydroxyurea (SWiTCH). Blood 2012;119:3925-3932.
77. Kassim AA, Galadanci NA, Pruthi S, et al. How I treat and manage strokes in sickle cell disease. Blood 2015;125:3401-3410.
78. Scothorn DJ, Price C, Schwartz D, et al. Risk of recurrent stroke in children with sickle cell disease receiving blood transfusion therapy for at least five years after initial stroke. J Pediatr 2002;140:348-354.
79. Hulbert ML, McKinstry RC, Lacey JL, et al. Silent cerebral infarcts occur despite regular blood transfusion therapy after first strokes in children with sickle cell disease. Blood 2011;117:772-779.
80. Bernaudin F, Verlhac S, Arnaud C, et al. Impact of early transcranial Doppler screening and intensive therapy on cerebral vasculopathy outcome in a newborn sickle cell anemia cohort. Blood 2011;117:1130-1140.
81. Pegelow CH, Macklin EA, Moser FG, et al. Longitudinal changes in brain magnetic resonance imaging findings in children with sickle cell disease. Blood 2002;99:3014-3018.
82. Schatz J, Brown RT, Pascual JM, et al. Poor school and cognitive functioning with silent cerebral infarcts and sickle cell disease. Neurology 2001;56:1109-1111.
83. Bernaudin F, Verlhac S, Freard F, et al. Multicenter prospective study of children with sickle cell disease: Radiographic and psychometric correlation. J Child Neurol 2000;15:333-343.
84. DeBaun MR, Gordon M, McKinstry RC, et al. Controlled trial of transfusions for silent cerebral infarcts in sickle cell anemia. N Engl J Med 2014;371:699-710.
85. Gladwin MT, Sachdev V, Jison ML, et al. Pulmonary hypertension as a risk factor for death in patients with sickle cell disease. N Engl J Med 2004;350:886-895.
86. Perronne V, Roberts-Harewood M, Bachir D, et al. Patterns of mortality in sickle cell disease in adults in France and England. Hematol J 2002;3:56-60.
87. Steiner CA, Miller JL. Sickle Cell Disease Patients in U.S. Hospitals, 2004: Statistical Brief #21. Rockville, MD: Healthcare Cost and Utilization Project (HCUP) Statistical Briefs; 2006.
88. Castro O, Hoque M, Brown BD. Pulmonary hypertension in sickle cell disease: Cardiac catheterization results and survival. Blood 2003;101:1257-1261.
89. De Castro LM, Jonassaint JC, Graham FL, et al. Pulmonary hypertension associated with sickle cell disease: Clinical and laboratory endpoints and disease outcomes. Am J Hematol 2008;83:19-25.
90. Sutton LL, Castro O, Cross DJ, et al. Pulmonary hypertension in sickle cell disease. Am J Cardiol 1994;74:626-628.
91. Machado RF, Anthi A, Steinberg MH, et al. N-terminal pro-brain natriuretic peptide levels and risk of death in sickle cell disease. JAMA 2006;296:310-318.
92. Machado RF, Hildesheim M, Mendelsohn L, et al. NT-pro brain natriuretic peptide levels and the risk of death in the cooperative study of sickle cell disease. Br J Haematol 2011;154:512-520.
93. Boyd JH, Macklin EA, Strunk RC, et al. Asthma is associated with increased mortality in individuals with sickle cell anemia. Haematologica 2007;92:1115-1118.
94. Morris CR. Asthma management: Reinventing the wheel in sickle cell disease. Am J Hematol 2009;84:234-241.
95. Boyd JH, Moinuddin A, Strunk RC, et al. Asthma and acute chest in sickle-cell disease. Pediatr Pulmonol 2004;38:229-232.
96. Nordness ME, Lynn J, Zacharisen MC, et al. Asthma is a risk factor for acute chest syndrome and cerebral vascular accidents in children with sickle cell disease. Clin Mol Allergy 2005;3:2.
97. Knight-Madden JM, Barton-Gooden A, Weaver SR, et al. Mortality, asthma, smoking and acute chest syndrome in young adults with sickle cell disease. Lung 2013;191:95-100.
98. Kassim AA, Payne AB, Rodeghier M, et al. Low forced expiratory volume is associated with earlier death in sickle cell anemia. Blood 2015;126:1544-1550.
99. Ghosh S, Adisa OA, Chappa P, et al. Extracellular hemin crisis triggers acute chest syndrome in sickle mice. J Clin Invest 2013;123:4809-4820.
100. Adisa OA, Hu Y, Ghosh S, et al. Association between plasma free haem and incidence of vaso-occlusive episodes and acute chest syndrome in children with sickle cell disease. Br J Haematol 2013;162:702-705.
101. Morris CR. New strategies for the treatment of pulmonary hypertension in sickle cell disease: the rationale for arginine therapy. Treatments Respir Med 2006;5:31-45.
102. Strouse JJ, Lanzkron S, Urrutia V. The epidemiology, evaluation and treatment of stroke in adults with sickle cell disease. Expert Rev Hematol 2011;4:597-606.
103. Steen RG, Miles MA, Helton KJ, et al. Cognitive impairment in children with hemoglobin SS sickle cell disease: Relationship to MR imaging findings and hematocrit. AJNR Am J Neuroradiol 2003;24:382-389.
104. Hogan AM, Pit-ten Cate IM, Vargha-Khadem F, et al. Physiological correlates of intellectual function in children with sickle cell disease: Hypoxaemia, hyperaemia and brain infarction. Dev Sci 2006;9:379-387.
105. Steen RG, Fineberg-Buchner C, Hankins G, et al. Cognitive deficits in children with sickle cell disease. J Child Neurol 2005;20:102-107.
106. Vichinsky EP, Neumayr LD, Gold JI, et al. Neuropsychological dysfunction and neuroimaging abnormalities in neurologically intact adults with sickle cell anemia. JAMA 2010;303:1823-1831.
107. Ballas SK. Neurocognitive complications of sickle cell anemia in adults. JAMA 2010;303:1862-1863.
108. McClish DK, Penberthy LT, Bovbjerg VE, et al. Health related quality of life in sickle cell patients: the PiSCES project. Health Qual Life Outcomes 2005;3:50.
109. Powars DR, Elliott-Mills DD, Chan L, et al. Chronic renal failure in sickle cell disease: Risk factors, clinical course, and mortality. Ann Intern Med 1991;115:614-620.
110. McClellan AC, Luthi JC, Lynch JR, et al. High one year mortality in adults with sickle cell disease and end-stage renal disease. Br J Haematol 2012;159:360-367.
111. Bhathena DB, Sondheimer JH. The glomerulopathy of homozygous sickle hemoglobin (SS) disease: Morphology and pathogenesis. J Am Soc Nephrol 1991;1:1241-1252.
112. Haymann JP, Stankovic K, Levy P, et al. Glomerular hyperfiltration in adult sickle cell anemia: A frequent hemolysis associated feature. Clin J Am Soc Nephrol 2010;5:756-761.
113. Thompson J, Reid M, Hambleton I, et al. Albuminuria and renal function in homozygous sickle cell disease: Observations from a cohort study. Arch Intern Med 2007;167:701-708.
114. Nath KA, Grande JP, Croatt AJ, et al. Transgenic sickle mice are markedly sensitive to renal ischemia-reperfusion injury. Am J Pathol 2005;166:963-972.
115. Juncos JP, Grande JP, Croatt AJ, et al. Early and prominent alterations in hemodynamics, signaling, and gene expression following renal ischemia in sickle cell disease. Am J Physiol Renal Physiol 2010;298:F892-899.
116. Nath KA, Grande JP, Haggard JJ, et al. Oxidative stress and induction of heme oxygenase-1 in the kidney in sickle cell disease. Am J Pathol 2001;158:893-903.
117. Nath KA, Hebbel RP. Sickle cell disease: Renal manifestations and mechanisms. Nat Rev Nephrol 2015;11:161-171.
118. Zemel BS, Kawchak DA, Ohene-Frempong K, et al. Effects of delayed pubertal development, nutritional status, and disease severity on longitudinal patterns of growth failure in children with sickle cell disease. Pediatr Res 2007;61:607-613.
119. Olambiwonnu NO, Penny R, Frasier SD. Sexual maturation in subjects with sickle cell anemia: Studies of serum gonadotropin concentration, height, weight, and skeletal age. J Pediatr 1975;87:459-464.
120. Smith-Whitley K. Reproductive issues in sickle cell disease. Blood 2014;124:3538-3543.
121. Oteng-Ntim E, Meeks D, Seed PT, et al. Adverse maternal and perinatal outcomes in pregnant women with sickle cell disease: Systematic review and meta-analysis. Blood 2015;125:3316-3325.
122. Parshad O, Stevens MC, Preece MA, et al. The mechanism of low testosterone levels in homozygous sickle-cell disease. West Indian Med J 1994;43:12-14.
123. Li M, Fogarty J, Whitney KD, et al. Repeated testicular infarction in a patient with sickle cell disease: A possible mechanism for testicular failure. Urology 2003;62:551
124. Adeyoju AB, Olujohungbe AB, Morris J, et al. Priapism in sickle-cell disease; incidence, risk factors and complications - An international multicentre study. BJU Int 2002;90:898-902.
125. Madu AJ, Ubesie A, Ocheni S, et al. Priapism in homozygous sickle cell patients: Important clinical and laboratory associations. Med Princ Pract 2014;23:259-263.
126. Osegbe DN, Akinyanju O, Amaku EO. Fertility in males with sickle cell disease. Lancet 1981;2:275-276.
127. Berthaut I, Guignedoux G, Kirsch-Noir F, et al. Influence of sickle cell disease and treatment with hydroxyurea on sperm parameters and fertility of human males. Haematologica 2008;93:988-993.
128. Jones KM, Niaz MS, Brooks CM, et al. Adverse effects of a clinically relevant dose of hydroxyurea used for the treatment of sickle cell disease on male fertility endpoints. Int J Environ Res Public Health 2009;6:1124-1144.
129. Dunne GD, Joseph RR. Fertility in hemoglobin S-S and hemoglobin S-C disease. Fertil Steril 1970;21:630-634.
130. Samuels-Reid JH, Scott RB, Brown WE. Contraceptive practices and reproductive patterns in sickle cell disease. J Natl Med Assoc 1984;76:879-883.
131. Malinowski AK, Shehata N, D'Souza R, et al. Prophylactic transfusion for pregnant women with sickle cell disease: A systematic review and meta-analysis. Blood 2015. [Epub ahead of print]
132. Johnson FL, Look AT, Gockerman J, et al. Bone-marrow transplantation in a patient with sickle-cell anemia. N Engl J Med 1984;311:780-783.
133. Vermylen C, Fernandez Robles E, Ninane J, et al. Bone marrow transplantation in five children with sickle cell anaemia. Lancet 1988;1:1427-1428.
134. Ferster A, De Valck C, Azzi N, et al. Bone marrow transplantation for severe sickle cell anaemia. Br J Haematol 1992;80:102-105.
135. Johnson FL, Mentzer WC, Kalinyak KA, et al. Bone marrow transplantation for sickle cell disease. The United States experience. Am J Pediatr Hematol Oncol 1994;16:22-26.
136. Vermylen C, Cornu G. Bone marrow transplantation for sickle cell disease. The European experience. Am J Pediatr Hematol Oncol 1994;16:18-21.
137. Walters MC, Patience M, Leisenring W, et al. Bone marrow transplantation for sickle cell disease. N Engl J Med 1996;335:369-376.
138. van Besien K, Bartholomew A, Stock W, et al. Fludarabine-based conditioning for allogeneic transplantation in adults with sickle cell disease. Bone Marrow Transplant 2000;26:445-449.
139. Iannone R, Casella JF, Fuchs EJ, et al. Results of minimally toxic nonmyeloablative transplantation in patients with sickle cell anemia and beta-thalassemia. Biol Blood Marrow Transplant 2003;9:519-528.
140. Hsieh MM, Kang EM, Fitzhugh CD, et al. Allogeneic hematopoietic stem-cell transplantation for sickle cell disease. N Engl J Med 2009;361:2309-2317.
141. Hsieh MM, Fitzhugh CD, Weitzel RP, et al. Nonmyeloablative HLA-matched sibling allogeneic hematopoietic stem cell transplantation for severe sickle cell phenotype. JAMA 2014;312:48-56.
142. Mentzer WC, Heller S, Pearle PR, et al. Availability of related donors for bone marrow transplantation in sickle cell anemia. Am J Pediatr Hematol Oncol 1994;16:27-29.
143. Bolanos-Meade J, Fuchs EJ, Luznik L, et al. HLA-haploidentical bone marrow transplantation with posttransplant cyclophosphamide expands the donor pool for patients with sickle cell disease. Blood 2012;120:4285-4291.
144. Grosse SD, Odame I, Atrash HK, et al. Sickle cell disease in Africa: A neglected cause of early childhood mortality. Am J Prev Med 2011;41:S398-405.