Sickle cell disease (SCD) affects nearly 300,000 newborns annually worldwide, with 80% born in Africa. Sickle cell nephropathy (SCN) affects 5–18% of patients with SCD and contributes significantly to morbidity and mortality. Identifying SCN-associated factors would promote effective clinical management. We conducted a global systematic review in accordance with the Preferred Reporting Items for Systematic Review and Meta-Analysis guidelines (Prospective Register of Systematic Reviews, registration number: CRD42020185763) to explore clinical and genetic correlates of SCN. We sought after cohort, case–control, and cross-sectional studies published up to December 31, 2024 that reported on clinical and/or genetic predictors of SCN in different populations globally. A total of 70 hospital-based study articles were finally included, with a leading percentage (45.7%) of the included studies performed in the United States, whereas 24.3% were from Sub-Saharan Africa. Most had a cross-sectional design (68.6%) involving children and adults. Genetic studies (17/70) identified associations with α-thalassemia, APOL1, and HMOX1 genes. The only genome-wide association study identified six suggestive variants in CRYL1, VWF, ADAMTS7, LRP1B, linc02288, and FPGT-TNNI3K/TNNI3K among adult patients. In conclusion, this systematic review (1) unpacks and highlights the role of clinical, genetic, and biochemical factors in the pathogenesis and progression of SCN and (2) reveals the consistent association of SCN with the 3.7 Kb deletion in HBA and variants in APOL1 and HMOX1 genes. This systematic review underscores the paucity of data from Africa, emphasizing the need for large-scale prospective studies on African SCN cohorts. Our findings also provide a foundation for the early identification of individuals at risk for SCN and the avenues for clinical and public health management strategies. To the best of our knowledge, this is the first systematic review summarizing risk factors for kidney dysfunction in SCD populations worldwide, which includes, specifically, a meta-analysis for APOL1 association with albuminuria.
Get full access to this article
View all access options for this article.
References
1.
AbanI, BaddamS, HilliardL, et al.Severe anemia early in life as a risk factor for sickle-cell kidney disease. BLOOD, 2017; 129(3):385–387; doi: 10.1182/blood-2016-09-738104
2.
AdebayoOC, Van den HeuvelLP, OlowuWA, et al.Sickle cell nephropathy: insights into the pediatric population. Pediatr Nephrol, 2022a;37(6):1231–1243; doi: 10.1007/s00467-021-05126-4
3.
AdebayoO, BetukumesuD, NkoyA, et al.Clinical and genetic factors are associated with kidney complications in African children with sickle cell anaemia. Br J Haematol, 2022b;196(1):204–214; doi: 10.1111/bjh.17832
4.
AleemA.Proteinuria in adult Saudi patients with sickle cell disease is not associated with identifiable risk factors. Saudi J Kidney Dis Transpl. , 2010; 21(5):903–908.
5.
AlexanderN, HiggsD, DoverG, et al.Are there clinical phenotypes of homozygous sickle cell disease?. Br J Haematol, 2004; 126(4):606–611; doi: 10.1111/j.1365-2141.2004.05025.x
6.
Al-MusawaF, Al-SaqladiA. Prevalence and correlates of microalbuminuria in Yemeni children with sickle cell disease. Saudi J Kidney Dis Transpl, 2019; 30(4):832–842; doi: 10.4103/1319-2442.265459
7.
AloniM, NgiyuluR, EkuluP, et al.Glomerular hyperfiltration is strongly correlated with age in Congolese children with sickle cell anaemia. Acta Paediatr, 2017; 106(5):819–824; doi: 10.1111/apa.13784
8.
AlvarezO, ZillerueloG, WrightD, et al.Serum cystatin C levels in children with sickle cell disease. Pediatr Nephrol, 2006a;21(4):533–537; doi: 10.1007/s00467-006-0033-6
9.
AlvarezO, MontaneB, LopezG, et al.Early blood transfusions protect against microalbuminuria in children with sickle cell disease. Pediatr Blood Cancer, 2006b;47(1):71–76; doi: 10.1002/pbc.20645
10.
AlzahraniY, AlgarniM, AlnashriM, et al.Prevalence and risk factors for microalbuminuria in children with sickle cell disease at King Abdulaziz University Hospital: A retrospective cross-sectional study. CUREUS, 2020; 12(1):e6638; doi: 10.7759/cureus.6638
11.
AlzahriM, MousaA, AlmomenAM, et al.Lactate dehydrogenase as a biomarker for early renal damage in patients with sickle cell disease. Saudi J Kidney Dis Transpl, 2015; 26(6):1161–1168; doi: 10.4103/1319-2442.168596
12.
Ashley-KochA, OkochaE, GarrettM, et al.MYH9 and APOL1 are both associated with sickle cell disease nephropathy. Br J Haematol, 2011; 155(3):386–394; doi: 10.1111/j.1365-2141.2011.08832.x
13.
AsnaniM, FraserR, ReidM. Higher rates of hemolysis are not associated with albuminuria in jamaicans with sickle cell disease. PLoS One, 2011; 6(4):e18863; doi: 10.1371/journal.pone.0018863
14.
AsnaniMR, BhattK, YoungerN, et al. Risky behaviours of Jamaican adolescents with sickle cell disease. Hematology, 2014; 19(7):373–379; doi: 10.1179/1607845413Y.0000000136
15.
AsnaniM, ReidM. Renal function in adult Jamaicans with homozygous sickle cell disease. Hematology, 2015a;20(7):422–428; doi: 10.1179/1607845414y.0000000213
16.
AsnaniM, ReidM. Cystatin C: a useful marker of glomerulopathy in sickle cell disease?. Blood Cells Mol Dis, 2015b;54(1):65–70; doi: 10.1016/j.bcmd.2014.07.018
17.
AsnaniM, SerjeantG, Royal-ThomasT, et al.Predictors of renal function progression in adults with homozygous sickle cell disease. Br J Haematol, 2016; 173(3):461–468; doi: 10.1111/bjh.13967
18.
AtagaK, DerebailV, ArcherD. The glomerulopathy of sickle cell disease. Am J Hematol, 2014; 89(9):907–914; doi: 10.1002/ajh.23762
19.
AtagaK, SarafS, DerebailV. The nephropathy of sickle cell trait and sickle cell disease. Nat Rev Nephrol, 2022; 18(6):361–377; doi: 10.1038/s41581-022-00540-9
20.
AygunB, MortierNA, SmeltzerMP, HankinsJS, WareRE. Glomerular hyperfiltration and albuminuria in children with sickle cell anemia. Pediatr Nephrol, 2011; 26(8):1285–1290; doi: 10.1007/s00467-011-1857-2
21.
BallasS. Sickle cell anemia with few painful crises is characterized by decreased red cell deformability and increased number of dense cells. Am J Hematol, 1991; 36(2):122–130; doi: 10.1002/ajh.2830360211
22.
BasakA, SankaranV. Regulation of the fetal hemoglobin silencing factor BCL11A. in. Cooley’s ANEMIA, 2016; doi: 10.1111/nyas.13024
23.
BeauchampT, ChildressJ. Principles of biomedical ethics, 6th ed.. Oxford University Press: New York; 2009.
24.
BectonL, KalpatthiR, RackoffE, et al.Prevalence and clinical correlates of microalbuminuria in children with sickle cell disease. Pediatr Nephrol, 2010; 25(8):1505–1511; doi: 10.1007/s00467-010-1536-8
25.
BelisárioA, Simões E SilvaA, MouraI, et al.; Recipient Epidemiology and Donor Evaluation Study (REDS-III) International Component Brazil. Estimated glomerular filtration rate in Brazilian adults with sickle cell disease: Results from the REDS-III multicenter cohort study. Ann Hematol, 2023; 102(5):1019–1027; doi: 10.1007/s00277-023-05150-4
26.
BergmannS, ZhengD, BarredoJ, et al.Renal kallikrein: A risk marker for nephropathy in children with sickle cell disease. J Pediatr Hematol Oncol, 2006; 28(3):147–153; doi: 10.1097/01.mph.0000203722.91189.9d
27.
BhaskarL.V.K.S. and PattnaikS.IL1RN VNTR Polymorphism and kidney damage in sickle cell anemia patients. J Nephropharmacol, 2023; 12(1):e10437; doi: 10.34172/npj.2022.10437
28.
BolarinwaRA, AkinladeKS, KutiMA, et al.Renal disease in adult Nigerians with sickle cell anemia: a report of prevalence, clinical features and risk factors. Saudi J Kidney Dis Transpl., 2012; 23(1):171–175.
29.
BukarA, SulaimanM, LaduA, et al.Chronic kidney disease amongst sickle cell anaemia patients at the University of Maiduguri Teaching Hospital, Northeastern Nigeria: A study of prevalence and risk factors. Mediterr J Hematol Infect Dis, 2019; 11(1):e2019010; doi: 10.4084/MJHID.2019.010
30.
BukiniD, deVriesJ, TreadwellM, et al.Exploring the role of shared decision making in the consent process for pediatric genomics research in Cameroon, Tanzania, and Ghana. AJOB Empir Bioeth, 2019; 10(3):182–189; doi: 10.1080/23294515.2019.1645759
31.
ChaturvediS, GhafuriD, GlassbergJ, et al.Rapidly progressive acute chest syndrome in individuals with sickle cell anemia: A distinct acute chest syndrome phenotype. Am J Hematol, 2016; 91(12):1185–1190; doi: 10.1002/ajh.24539
32.
ChineduO, TonasséW, AlbuquerqueD, et al.Polymorphisms in the heme oxygenase-1 and bone morphogenetic protein receptor type 1b genes and estimated glomerular filtration rate in Brazilian sickle cell anemia patients. Hematol Transfus Cell Ther, 2021; 43(2):165–170; doi: 10.1016/j.htct.2020.01.009
33.
CooperA, IlboudoH, AlibuV, et al.APOL1 renal risk variants have contrasting resistance and susceptibility associations with African trypanosomiasis. Elife, 2017; 6:e25461; doi: 10.7554/elife.25461
34.
DayT, DrasarE, FulfordT, et al.Association between hemolysis and albuminuria in adults with sickle cell anemia. Haematologica, 2012; 97(2):201–205; doi: 10.3324/haematol.2011.050336
35.
de VriesJ, LandouréG, WonkamA. Stigma in African genomics research: Gendered blame, polygamy, ancestry and disease causal beliefs impact on the risk of harm. Soc Sci Med, 2020; 258:113091; doi: 10.1016/j.socscimed.2020.113091
36.
Dennis-AntwiJA, Ohene-FrempongK, AnieKA, et al.Relation between religious perspectives and views on sickle cell disease research and associated public health interventions in Ghana. J Genet Couns, 2018; doi: 10.1007/s10897-018-0296-7
37.
DerebailV, ZhouQ, CicconeE, et al.Rapid decline in estimated glomerular filtration rate is common in adults with sickle cell disease and associated with increased mortality. Br J Haematol, 2019; 186(6):900–907; doi: 10.1111/bjh.16003
38.
EkeC, OkaforH, IbeB. Prevalence and correlates of microalbuminuria in children with sickle cell anaemia: Experience in a tertiary health facility in Enugu, Nigeria. Int J Nephrol, 2012; 2012:240173; doi: 10.1155/2012/240173
39.
EkrikpoU, MnikaK, EffaE, et al.Association of genetic polymorphisms of TGF-β1, HMOX1, and APOL1 With CKD in Nigerian patients with and without HIV. Am J Kidney Dis, 2020; 76(1):100–108; doi: 10.1053/j.ajkd.2020.01.006
40.
ElbalawyS, GadN, AlshwameenM, et al.Microalbuminuria as a predictor of early glomerular injury in children and adolescents with Sickle Cell Anaemia at King Salman Armed Forced Hospital, Tabuk, Saudi Arabia. Medical SCIENCE, 2019; 23(96):227–232.
41.
ErshlerWB, De CastroLM, PakbazZ, et al.Hemoglobin and End-Organ Damage in Individuals with Sickle Cell Disease. Curr Ther Res Clin Exp., 2023; 98:100696; doi: 10.1016/j.curtheres.2023.100696
42.
EsohK, WonkamA. A Evolutionary history of sickle-cell mutation: Implications for global genetic medicine. Hum Mol Genet, 2021; 30(R1):R119–R128; doi: 10.1093/hmg/ddab004
43.
EwuosoC, BerkmanB, WonkamA, et al.Should institutions fund the feedback of individual findings in genomic research? J Med Ethics, 2024; 50(8):569–574; doi: 10.1136/medethics-2021-107992
44.
EwuosoC, Cordeiro-RodriguesL, WonkamA, et al.Addressing exploitation and inequities in open science: A relational perspective. Dev World Bioeth, 2023; 23(4):331–343; doi: 10.1111/dewb.12378
45.
FalkR, JennetteJ. Renal disease. In: Sickle Cell Disease: Basic principles and Clinical Practice. Statpearls: 1994; pp. 673–680.
46.
FaulknerM, TurnerE, DeusJ, et al.Severe anemia: A risk factor for glomerular injury in sickle cell disease. J Natl Med Assoc, 1995; 87(3):209–213.
47.
GarrettM, SoldanoK, ErwinK, et al.Genome-wide meta-analysis identifies new candidate genes for sickle cell disease nephropathy. Blood Adv, 2023; 7(17):4782–4793; doi: 10.1182/bloodadvances.2022007451
48.
GbadegesinS. African Philosophy: Traditional Yoruba Philosophy and Contemporary African Realities. Peter Lang; 2009; pp. 27–60.
49.
GeardA, PuleG, Chetcha ChemegniB, et al.Clinical and genetic predictors of renal dysfunctions in sickle cell anaemia in Cameroon. Br J Haematol, 2017; 178(4):629–639; doi: 10.1111/bjh.14724
50.
GenoveseG, FriedmanD, RossM, et al.Association of Trypanolytic APOL1 variants with kidney disease in African Americans. Science, 2010; 329(5993):841–845; doi: 10.1126/science.1193032
51.
GenoveseG, TonnaS, KnobA, et al.A risk allele for focal segmental glomerulosclerosis in African Americans is located within a region containing APOL1 and MYH9. Kidney Int, 2010; 78(7):698–704; doi: 10.1038/ki.2010.251
52.
GhobrialE, Abdel-AzizH, KaddahA, et al.Urinary transforming growth factor beta-1 as a marker of renal dysfunction in sickle cell disease. Pediatr Neonatol, 2016; 57(3):174–180; doi: 10.1016/j.pedneo.2015.05.001
53.
GordeukVR, SachdevV, TaylorJG, et al.Relative systemic hypertension in patients with sickle cell disease is associated with risk of pulmonary hypertension and renal insufficiency. Am J Hematol, 2008; 83(1):15–18; doi: 10.1002/ajh.21016
54.
GosmanovaEO, ZaidiS, WanJY, et al.Prevalence and progression of chronic kidney disease in adult patients with sickle cell disease. J Investig Med., 2014; 62(5):804–807; doi: 10.1097/01.JIM.0000446836.75352.72
55.
GuaschA, CuaM, MitchW. Early detection and the course of glomerular injury in patients with sickle cell anemia. Kidney Int, 1996; 49(3):786–791; doi: 10.1038/ki.1996.109
56.
GuaschA, CuaM, YouW, et al.Sickle cell anemia causes a distinct pattern of glomerular dysfunction. Kidney Int, 1997; 51(3):826–833; doi: 10.1038/ki.1997.116
57.
GuaschA, ZayasCF, EckmanJR, et al.Evidence that microdeletions in the alpha globin gene protect against the development of sickle cell glomerulopathy in humans. J Am Soc Nephrol, 1999; 10(5):1014–1019; doi: 10.1681/ASN.V1051014
58.
HamidehD, RajV, HarringtonT, et al.Albuminuria correlates with hemolysis and NAG and KIM-1 in patients with sickle cell anemia. Pediatr Nephrol, 2014; 29(10):1997–2003.
59.
HassanM, Al-NaamaL, JawadS. Microalbuminuria among children and adolescents with sickle cell disease. Iraqi J Hematol, 2022; 11(2):103–103; doi: 10.4103/ijh.ijh_17_22
60.
HaymannJ, HammoudiN, Stankovic StojanovicK, et al.Renin-angiotensin system blockade promotes a cardio-renal protection in albuminuric homozygous sickle cell patients. Br J Haematol, 2017; 179(5):820–828; doi: 10.1111/bjh.14969
61.
HuC, KlopferE, RayP. Human Apolipoprotein 1 (APOL1) in cancer and chronic kidney disease. FEBS Lett, 2012; 586(7):947–955; doi: 10.1016/j.febslet.2012.03.002
62.
ImuetinyanB, OkoegualeM, EgberueG. Microalbuminuria in children with sickle cell anemia. Saudi J Kidney Dis Transpl, 2011; 22(4):733–738.
63.
ItokuaK, MakuloJ, LepiraF, et al.Albuminuria, serum antioxidant enzyme levels and markers of hemolysis and inflammation in steady state children with sickle cell anemia. BMC Nephrol, 2016; 17(1):178–176; doi: 10.1186/s12882-016-0398-0
64.
JegedeA. Culture and genetic screening in Africa. Dev World Bioeth, 2009; 9(3):128–137; doi: 10.1111/j.1471-8847.2009.00259.x
65.
Kambale-KombiP, Djang’eing’aR, Alworong’a OparaJ, et al.Renal abnormalities among sickle cell disease patients in a poor management setting: A survey in the democratic republic of the congo. Mediterr J Hematol Infect Dis, 2022; 14(1):e2022046; doi: 10.4084/MJHID.2022.046
66.
KasparC, BeachI, NewlinJ, et al.Hyperuricemia is associated with a lower glomerular filtration rate in pediatric sickle cell disease patients. Pediatr Nephrol, 2020; 35(5):883–889; doi: 10.1007/s00467-019-04432-2
67.
KatoG, GladwinM, SteinbergM. Deconstructing sickle cell disease: Reappraisal of the role of hemolysis in the development of clinical subphenotypes. Blood Rev, 2007; 21(1):37–47; doi: 10.1016/j.blre.2006.07.001
68.
KatoGJ, SteinbergMH, GladwinMT. Intravascular hemolysis and the pathophysiology of sickle cell disease. J Clin Invest, 2017; 127(3):750–760; doi: 10.1172/JCI89741
69.
KhanA, TurchinM, PatkiA, et al.Genome-wide polygenic score to predict chronic kidney disease across ancestries. Nat Med, 2022; 28(7):1412–1420; doi: 10.1038/s41591-022-01869-1
70.
KimaroF, JumanneS, SindatoE, et al.Prevalence and factors associated with renal dysfunction among children with sickle cell disease attending the sickle cell disease clinic at a tertiary hospital in Northwestern Tanzania. PLoS One, 2019; 14(6):e0218024–e0218024; doi: 10.1371/journal.pone.0218024
71.
KormannR, JannotA, NarjozC, et al.Roles of APOL1G1 and G2 variants in sickle cell disease patients: Kidney is the main target. Br J Haematol, 2017; 179(2):323–335; doi: 10.1111/bjh.14842
72.
LebensburgerJ, CutterG, HowardT, et al.Evaluating risk factors for chronic kidney disease in pediatric patients with sickle cell anemia. Pediatr Nephrol, 2017; 32(9):1565–1573; doi: 10.1007/s00467-017-3658-8
73.
MachilaN, Chunda-LiyokaC, ChabalaC. Prevalence and risk factors of chronic kidney disease in steady state sickle cell anaemia patients aged 5-16 years seen at the university teaching hospital, lusaka—zambia. Pediatric NEPHROLOGY, 2016; 31(10):1783–1783.
74.
Maier-RedelspergerM, LévyP, LionnetF, et al.Strong association between a new marker of hemolysis and glomerulopathy in sickle cell anemia. Blood Cells Mol Dis, 2010; 45(4):289–292; doi: 10.1016/j.bcmd.2010.08.001
75.
MakaniJ, SangedaR, NnoduO, et al.SickleInAfrica. The Lancet. Haematology, 2020; 7(2):e98–e99; doi: 10.1016/S2352-3026(20)30006-5
76.
MawandaM, SsenkusuJ, OdiitA, et al.Micro-albuminuria in Ugandan children with sickle cell anaemia: A cross-sectional study. Ann Trop Paediatr, 2011; 31(2):115–121; doi: 10.1179/1465328111y.0000000013
77.
McBurneyP, HanevoldC, HernandezC, et al.Risk factors for microalbuminuria in children with sickle cell anemia. J Pediatr Hematol Oncol, 2002; 24(6):473–477; doi: 10.1097/00043426-200208000-00013
78.
McKieK, HanevoldC, HernandezC, et al.Prevalence, prevention, and treatment of microalbuminuria and proteinuria in children with sickle cell disease. J Pediatr Hematol Oncol, 2007; 29(3):140–144; doi: 10.1097/mph.0b013e3180335081
79.
McPhearson YeeM, JabbarSF, OsunkwoI, et al.Chronic kidney disease and albuminuria in children with sickle cell disease. Clin J Am Soc Nephrol, 2011; 6(11):2628–2633; doi: 10.2215/cjn.01600211
80.
MoherD, LiberatiA, TetzlaffJ, et al.; PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med, 2009; 6(7):e1000097; doi: 10.1371/journal.pmed.1000097
81.
MohtatD, ThomasR, DuZ, et al.Urinary transforming growth factor beta-1 as a marker of renal dysfunction in sickle cell disease. Pediatr Nephrol, 2011; 26(2):275–280; doi: 10.1007/s00467-010-1677-9
82.
MorriceJ, MupfururirwaW, ChianumbaRI, et al.; Members of SPARCO Nigeria. Sickle cell disease in Africa: SickleInAfrica registry in Ghana, Nigeria and Tanzania. EJHaem, 2025; 6(3):e70044; doi: 10.1002/jha2.70044
83.
MunungN, KamgaK, TreadwellM, et al.Perceptions and preferences for genetic testing for sickle cell disease or trait: A qualitative study in Cameroon, Ghana and Tanzania. European Journal of Human Genetics: EJHG, 2024; 32(10):1307–1313; doi: 10.1038/s41431-024-01553-7(a).
84.
MunungN, NembawareV, de VriesJ, et al.Establishing a multi-country sickle cell disease registry in Africa: Ethical considerations. Front Genet, 2019; 10:943; doi: 10.3389/fgene.2019.00943
85.
MunungN, NembawareV, Osei-TutuL, et al.; SickleInAfrica ELSI WG. Assent, parental consent and reconsent for health research in Africa: Thematic analysis of national guidelines and lessons from the SickleInAfrica registry. BMC Med Ethics, 2022; 23(1):130; doi: 10.1186/s12910-022-00843-3
86.
MunungN, RoyalC, de KockC, et al.Genomics and health data governance in Africa: Democratize the use of big data and popularize public engagement. Hastings Cent Rep, 2024; 54 (Suppl 2):S84–S92; doi: 10.1002/hast.4933
87.
MunungN, StauntonC, MazibukoO, et al.Data protection legislation in Africa and pathways for enhancing compliance in big data health research. Health Res Policy Syst, 2024; 22(1):145; doi: 10.1186/s12961-024-01230-7
88.
MunungN, TreadwellM, KamgaK, et al.Caught between pity, explicit bias, and discrimination: A qualitative study on the impact of stigma on the quality of life of persons living with sickle cell disease in three African countries. Qual Life Res, 2024; 33(2):423–432; doi: 10.1007/s11136-023-03533-8
NdourE, MnikaK, Guèye TallF, et al.Effects of Senegal haplotype (Xmn1-rs7412844), alpha-thalassemia (3.7kb HBA1/HBA2 deletion), NPRL3-rs11248850 and BCL11A-rs4671393 variants on sickle cell nephropathy. Int J Biochem Mol Biol, 2022; 13(2):5–16.
91.
Ngo-BitounguiV, BelingaS, MnikaK, et al.Investigations of kidney dysfunction-related gene variants in sickle cell disease patients in Cameroon (Sub-Saharan Africa). Front Genet, 2021; 12:595702–595702; doi: 10.3389/fgene.2021.595702
92.
NissO, LaneA, AsnaniM, et al.Progression of albuminuria in patients with sickle cell anemia: A multicenter, longitudinal study. Blood Adv, 2020; 4(7):1501–1511; doi: 10.1182/bloodadvances.2019001378
93.
NnajiU, OgokeC, OkaforH, et al.Sickle cell nephropathy and associated factors among asymptomatic children with sickle cell anaemia. Int J Pediatr, 2020; 2020:1286432; doi: 10.1155/2020/1286432
94.
NnoduO, MunungN, ChirandeL, et al.; SickleInAfrica Consortium. Acceptability, barriers and facilitators of using dried blood spots-point-of-care testing for sickle cell disease in Africa: An implementation science protocol for a multinational qualitative study. BMJ Open, 2024; 14(11):e089056; doi: 10.1136/bmjopen-2024-089056
95.
NolanV, MaQ, CohenH, et al.Estimated glomerular filtration rate in sickle cell anemia is associated with polymorphisms of bone morphogenetic protein receptor 1B. Am J Hematol, 2007; 82(3):179–184; doi: 10.1002/ajh.20800
96.
NovelliEM, HildesheimM, RosanoC, et al.Elevated pulse pressure is associated with hemolysis, proteinuria and chronic kidney disease in sickle cell disease. PLoS One, 2014; 9(12):e114309; doi: 10.1371/journal.pone.0114309
97.
OchekeI, MohamedS, OkpeE, et al.Microalbuminuria risks and glomerular filtration in children with sickle cell anaemia in Nigeria. Ital J Pediatr, 2019; 45(1):143; doi: 10.1186/s13052-019-0720-0
98.
OjewunmiO, AdeyemoT, OyetunjiA, et al.The genetic dissection of fetal haemoglobin persistence in sickle cell disease in Nigeria. Hum Mol Genet, 2024; 33(10):919–929; doi: 10.1093/hmg/ddae014
99.
OkamM, ShaykevichS, EbertB, et al.National trends in hospitalizations for sickle cell disease in the United States following the FDA approval of hydroxyurea, 1998-2008. Med Care, 2014; 52(7):612–618; doi: 10.1097/mlr.0000000000000143
100.
PattaroC.Genome-wide association studies of albuminuria: Towards genetic stratification in diabetes?. J Nephrol, 2018; 31(4):475–487; doi: 10.1007/s40620-017-0437-3
101.
PellenC, MunungN, ArmondA, et al.Data management and sharing. J Clin Epidemiol, 2025; 180:111680; doi: 10.1016/j.jclinepi.2025.111680
102.
PielF, PatilA, HowesR, et al.Global epidemiology of sickle haemoglobin in neonates: A contemporary geostatistical model based map and population estimates. Lancet, 2013; 381(9861):142–151; doi: 10.1016/s0140-6736(12)61229-x
103.
PielFB, WilliamsTN. Subphenotypes of sickle cell disease in Africa. Blood, 2017; 130(20):2157–2158; doi: 10.1182/blood-2017-10-808550
104.
PlattO, BrambillaD, RosseW, et al.Mortality in sickle cell disease—life expectancy and risk factors for early death. N Engl J Med, 1994; 330(23):1639–1644; doi: 10.1056/nejm199406093302303
105.
PowarsD, ChanL, HitiA, et al.Outcome of sickle cell anemia: A 4-decade observational study of 1056 patients. Medicine (Baltimore), 2005; 84(6):363–376; doi: 10.1097/01.md.0000189089.45003.52
106.
PowarsD, Elliott-MillsD, ChanL, et al.Chronic renal failure in sickle cell disease: Risk factors, clinical course, and mortality. Ann Intern Med, 1991; 115(8):614–620; doi: 10.7326/0003-4819-115-8-614
107.
RanqueB, MenetA, DiopI, et al.Early renal damage in patients with sickle cell disease inn sub-Saharan Africa: A multinational, prospective, cross-sectional study. The Lancet Haematology, 2014; 1(2):e64–e73; doi: 10.1016/s2352-3026(14)00007-6
RogerC, LionnetF, MattioniS, et al.Risk factors for CKD stage II onset in a prospective cohort of homozygous sickle cell adults. Am J Hematol, 2021; 96(9):1147–1155; doi: 10.1002/ajh.26264
111.
SarafS, LinX, LeeG, et al.Urinary ceruloplasmin concentration predicts development of kidney disease in sickle cell disease patients. BLOOD, 2016; 128(22):4865–4865; doi: 10.1182/blood.V128.22.4865.4865
112.
SarafSL, MolokieRE, NouraieM, et al.Differences in the clinical and genotypic presentation of sickle cell disease around the world. Paediatr Respir Rev, 2014a;15(1):4–12; doi: 10.1016/j.prrv.2013.11.003
113.
SarafS, ZhangX, KaniasT, et al.Haemoglobinuria is associated with chronic kidney disease and its progression in patients with sickle cell anaemia. Br J Haematol, 2014b;164(5):729–739; doi: 10.1111/bjh.12690
114.
SarafS, SysolJ, SusmaA, et al.Progressive glomerular and tubular damage in sickle cell trait and sickle cell anemia mouse models. Transl Res, 2018a;197:1–11; doi: 10.1016/j.trsl.2018.01.007
115.
SarafS, VinerM, RischallA, et al.HMOX1 and acute kidney injury in sickle cell anemia, in. Blood, 2018b;132(15):1621–1625; doi: 10.1182/blood-2018-05-853929
116.
SarafS, ZhangX, ShahB, et al.Genetic variants and cell-free hemoglobin processing in sickle cell nephropathy. Haematologica, 2015; 100(10):1275–1284; doi: 10.3324/haematol.2015.124875
117.
SchaeferB, FlanaganJ, AlvarezO, et al.Genetic modifiers of white blood cell count, Albuminuria and Glomerular filtration rate in children with sickle cell Anemia. PLoS One, 2016; 11(10):e0164364; doi: 10.1371/journal.pone.0164364
118.
SchaefferE, GuzzoT, FurgeK, et al.Renal medullary carcinoma: Molecular, pathological and clinical evidence for treatment with topoisomerase-inhibiting therapy. BJU Int, 2010; 106(1):62–65; doi: 10.1111/j.1464-410x.2009.09139.x
Silva JuniorG, LibórioA, VieiraA, et al.Evaluation of renal function in sickle cell disease patients in Brazil. Braz J Med Biol Res, 2012; 45(7):652–655; doi: 10.1590/S0100-879X2012007500079
121.
SohaniZ, MeyreD, de SouzaR, et al.Assessing the quality of published genetic association studies in meta-analyses: The quality of genetic studies (Q-Genie) tool. BMC Genet, 2015; 16:50; doi: 10.1186/s12863-015-0211-2
122.
SteinbergM. Genetic etiologies for phenotypic diversity in sickle cell anemia. ScientificWorldJournal, 2009; 9:46–67; doi: 10.1100/tsw.2009.10
123.
SteinbergMH, KumarS, MurphyGJ, et al.Sickle cell disease in the era of precision medicine: looking to the future. Expert Rev Precis Med Drug Dev, 2019; 4(6):357–367; doi: 10.1080/23808993.2019.1688658
124.
SundaramN, BennettM, WilhelmJ, et al.Biomarkers for early detection of sickle nephropathy. Am J Hematol, 2011; 86(7):559–566; doi: 10.1002/ajh.22045
125.
TshiloloL, TomlinsonG, WilliamsT, et al.; REACH Investigators. Hydroxyurea for children with sickle cell anemia in Sub-Saharan Africa. N Engl J Med, 2019; 380(2):121–131; doi: 10.1056/NEJMoa1813598
126.
TzurS, RossetS, ShemerR, et al.Missense mutations in the APOL1 gene are highly associated with end stage kidney disease risk previously attributed to the MYH9 gene. Hum Genet, 2010; 128(3):345–350; doi: 10.1007/s00439-010-0861-0
127.
UrioF, NkyaS, RooksH, et al.F cell numbers are associated with an X-linked genetic polymorphism and correlate with haematological parameters in patients with sickle cell disease. Br J Haematol, 2020; 191(5):888–896; doi: 10.1111/bjh.17102
128.
VoskaridouE, TerposE, MichailS, et al.Early markers of renal dysfunction in patients with sickle cell/beta-thalassemia. Kidney Int, 2006; 69(11):2037–2042; doi: 10.1038/sj.ki.5000248
129.
WareR, de MontalembertM, TshiloloL, et al.Sickle cell disease. Lancet, 2017; 390(10091):311–323; doi: 10.1016/s0140-6736(17)30193-9
WonkamA, de VriesJ. Returning incidental findings in African genomics research. Nat Genet, 2020; 52(1):17–20; doi: 10.1038/s41588-019-0542-4
132.
WonkamA, EsohK, LevineR, et al.FLT1 and other candidate fetal haemoglobin modifying loci in sickle cell disease in African ancestries. Nat Commun, 2025; 16(1):2092; doi: 10.1038/s41467-025-57413-5
133.
WonkamA, de VriesJ, RoyalCD, et al.Would you terminate a pregnancy affected by sickle cell disease? Analysis of views of patients in Cameroon. J Med Ethics, 2014; 40(9):615–620; doi: 10.1136/medethics-2013-101392
134.
WuH, LarsenC, Hernandez-ArroyoC, et al.AKI and collapsing glomerulopathy associated with covid-19 and apol1 high-risk genotype. J Am Soc Nephrol, 2020; 31(8):1688–1695; doi: 10.1681/asn.2020050558
135.
XuJ, GarrettM, SoldanoK, et al.Clinical and metabolomic risk factors associated with rapid renal function decline in sickle cell disease. Am J Hematol, 2018; 93(12):1451–1460; doi: 10.1002/ajh.25263
136.
XuY, MagwangaR, JinD, et al.Comparative transcriptome analysis reveals evolutionary divergence and shared network of cold and salt stress response in diploid D-genome cotton. BMC Plant Biol, 2020; 20(1):518; doi: 10.1186/s12870-020-02726-4
137.
YeruvaL, PaulY, OnealP, et al.Renal failure in sickle cell disease: Prevalence, predictors of disease, mortality and effect on length of hospital stay. HEMOGLOBIN, 2016; 40(5):295–299; doi: 10.1080/03630269.2016.1224766
138.
ZahrRS, RampersaudE, KangG, et al.Children with sickle cell anemia and APOL1 genetic variants develop albuminuria early in life. Haematologica, 2019; 104(9):e385–e387; doi: 10.3324/haematol.2018.212779
