|Year : 2018 | Volume
| Issue : 1 | Page : 22-28
Clinical features and outcome of sickle cell anemia in a tertiary center: A retrospective cohort study
Abdulrahman Musaad Alhumaid1, Abdulmalek Suliman Aleidi1, Abdullelah Saleh Alfakhri1, Naif Khalil Alosaimi1, Yosra Z Ali2, Mohsen Saadi Alzahrani2
1 King Saud Bin Abdulaziz University for Health Sciences, College of Medicine, Riyadh, Kingdom of Saudi Arabia
2 Department of Hematology, King Saud Bin Abdulaziz University for Health Sciences, National Guard Health Affairs, Riyadh, Kingdom of Saudi Arabia
|Date of Web Publication||22-Mar-2018|
Dr. Mohsen Saadi Alzahrani
King Saud Bin Abdulaziz University for Health Sciences, Department of Hematology, National Guard Health Affairs, P.O. Box 22490, Riyadh 11426
Kingdom of Saudi Arabia
Source of Support: None, Conflict of Interest: None
Introduction: Sickle cell anemia (SCA) is one of the most common genetic diseases worldwide. Patients with SCA present with varied clinical features and complications that may affect many organs in the human body. There are few treatment options for SCA, and patient responses vary; the only curative therapy is a stem cell transplant or gene therapy. We seek to study the clinical features and treatment options for patients with sickle cell disease treated in King Abdulaziz Medical City, Riyadh.
Methods: This study was a retrospective cohort study of all adult SCA patients who were admitted to our institution during the period from 1983 to 2016. Data were entered into Excel spreadsheets and managed with SPSS. Chi-square test was used to compare responses to therapy and in patients with different presentations.
Results: A total of 106 patients with sickle cell disease were included in this study. The percentages with respect to hospital admissions per year were as follows: 34.9% (37 patients) were never admitted, 26.4% (28 patients) were admitted fewer than 2 times, 24.5% (26 patients) were admitted 3–5 times, and 13.2% (14 patients) were admitted more than 5 times. The number of complications was used to measure the severity of the disease. The disease severity was higher in males than in females (67.3% vs. 32.7%, respectively; P = 0.018). The disease severity was higher in those who were born in the Western and Southwestern areas than in other areas (84.2% vs. 15.8%, respectively; P = 0.007). Hydroxyurea significantly reduced the severity of SCA with a P = 0.002.
Conclusion: Our study showed that vaso-occlusive crisis was the most common complication and indication for hospital admission. Treatment with hydroxyurea led to a significant reduction in the number of hospital admissions.
Keywords: Anemia, complication, hemoglobin, hemoglobin SS, hospitalization, sickle cell, sickle cell disease
|How to cite this article:|
Alhumaid AM, Aleidi AS, Alfakhri AS, Alosaimi NK, Ali YZ, Alzahrani MS. Clinical features and outcome of sickle cell anemia in a tertiary center: A retrospective cohort study. J Appl Hematol 2018;9:22-8
|How to cite this URL:|
Alhumaid AM, Aleidi AS, Alfakhri AS, Alosaimi NK, Ali YZ, Alzahrani MS. Clinical features and outcome of sickle cell anemia in a tertiary center: A retrospective cohort study. J Appl Hematol [serial online] 2018 [cited 2023 Sep 22];9:22-8. Available from: https://www.jahjournal.org/text.asp?2018/9/1/22/228331
| Introduction|| |
Sickle cell anemia (SCA) is one of the most common genetic diseases in the world. It is an autosomal recessive condition, in which the normally freely flowing cytosol of red cells is viscous, making them much less deformable and affecting their ability to traverse narrow capillary beds., These irregularly shaped blood cells can get stuck in blood vessels, blocking or slowing blood flow and oxygen to the organs, and causing pain and organs damage.,,, The mutation in the β-globin chain results from a substitution of valine for glutamic acid at the sixth codon.,, The prevalence is not limited to a certain race; however, the disease mostly affects African populations and those of African descent in many other countries.,,,,,, The prevalence of sickle cell disease differs in different parts of Saudi Arabia, with the highest prevalence in the eastern province followed by the Southwestern provinces and the severity of the disease differs from region to another., Currently, approximately 61,000 individuals have the disease in Saudi Arabia. Sickle cell disease is commonly observed in clinical practice in Saudi Arabia. The purpose of this research is to study the variations in clinical features and treatment options for patients with sickle cell disease treated at King Abdulaziz Medical City, Riyadh.
| Methods|| |
The study was a retrospective cohort study, and we targeted all patients diagnosed with SCA from the year 1983–2016. All patients who admitted with a diagnosis of SCA to King Abdulaziz Medical City in Riyadh were included in this study. A data collection sheet was formulated by the researchers, and it included the following variables: patient demographic data, diagnostic and laboratory data, clinical data, and disease complications. The data were collected from patient files as well as from the electronic medical record system. We used a unique identification number for every patient instead of name or medical record number. The data were kept confidential and stored in a safe place. Data were entered into Excel spreadsheets and then managed with SPSS (Statistical package for the social Sciences) version 22 using descriptive methods: Mean and standard deviation for numerical variables and percentages and frequencies for all categorical variables. Chi-square test was used to compare responses to therapy and in patients with different presentations.
| Results|| |
We included 106 patients with sickle cell disease diagnosed during the period from 1983 to 2015. Male patients were more prevalent in this population (55.7%) compared to female patients (44.3%). The median age was 27 years. Of the enrolled patients, 30.2% (32 patients) were diagnosed with SCA hemoglobin type SS and 1.9% (2 patients) with SCA hemoglobin type SC. The majority of patients in this study were from the Southwestern region (38.7%; 41 patients), followed by 13.2% (14 patients) from the Western region, 14.2% (15 patients) from the Central region, 7.5% (8 patients) from the Eastern region, 0.9% (1 patient) from the Northern region, and 25.5% (27 patients) with no available data of city of origin. The unmarried patients made up 59.4% (63 patients) of the cohort and 32.1% (34 patients) of patients were married. A total of 49.1% (52 patients) had a family history of SCA or sickle cell trait. [Table 1] shows the summary of demographic data.
Disease complications are shown in [Table 2]. A total of 30.2% of patients (32 patients) presented with acute painful crisis as the initial manifestation, 28.3% (30 patients) presented with anemia, and 1.9% (2 patients) presented with dactylitis. The average number of hospital admissions per year for the last 3 years at the time of data collection was as follows: 34.9% (37 patients) of patients were not admitted, 26.4% (28 patients) were admitted fewer than 2 times, 24.5% (26 patients) were admitted 3–5 times, and 13.2% (14 patients) were admitted more than 5 times [Graph 1]. The number of admissions to the hospital was used as an indicator of disease severity. Veno-occlusive disease was seen in 84% (89 patients) of patients and was the most common complication. Of this group, 23.6% of patients manifested with fewer than 3 instances per year, 22.5% with 3–5 instances per year, and 25.8% with more than 5 instances per year. Acute chest syndrome was seen in 43.4% of patients (46 patients). Of this group, 21.8% of patients experienced 1 instance, 26.1% had 2 instances, and 13% had 3 or more instances. Stroke was seen in 1.9% of patients (2 patients) as a single stroke instance; one was ischemic and the other was hemorrhagic at ages 22 and 49 years old, respectively. Seizures were seen in 5.7% of patients (6 patients). Avascular necrosis (AVN) of joints was seen in 21.7% of patients (23 patients). Seventeen patients (73.9%) had 1 joint involvement, and 26.1% (6 patients) had 2 or more joints involvements. Joint replacement as treatment for AVN was performed for 13.2% (14 patients) of the entire patient population. Osteomyelitis was seen in 2.3% of patients (13 patients); 4.7% (5 patients) had an aplastic crisis and 20.8% (22 patients) had a hemolytic crisis. Furthermore, 10.4% of patients (11 patients) were found to have pulmonary hypertension, 6.6% (7 patients) had splenic sequestration, 5.7% (6 patients) had a history of venous thrombosis, and 2.8% (3 patients) had hepatic sickling. Psychiatric complications were found in 4.7% of patients (5 patients) and 80% of these (4 patients) had experienced depression [Graph 2].
Treatment and responses
Different treatment modalities were used in our patient cohorts depending on the severity and complications. Hydroxyurea was used for 53.8% of patients (57 patients). The average number of admissions per year before starting hydroxyurea was 5 admissions per year; after starting hydroxyurea, we have observed a reduction in the admission rate to two admissions per year per patient, which may indicate a therapeutic response to hydroxyurea. Blood transfusions were frequently used in our group, with 10.4% of patients (11 patients) receiving regular monthly blood transfusions. The indications for blood transfusion were as follows: Recurrent uncontrolled painful vaso-occlusive crisis (VOC) crises in 17 patients, acute chest syndrome in 12 patients, stroke in 1 patient, and recurrent priapism in 1 patent. By contrast, approximately 37.7% of patients (40 patients) received occasional blood transfusions and the common indications for blood transfusions in this group were as follows: Painful crises in 40 patients, hemolytic crises in 17 patients, severe anemia in 13 patients, aplastic crises in 4 patients, and sequestration crises in 3 patients. A total of 14.2% (15 patients) were given iron chelation, 46.7% of which were compliant with the iron chelation therapy. Folic acid tablets were given to 80.2% of patients (85 patients) and 44.3% (47 patients) were on prophylactic antibiotics. We did not find accurate data regarding the vaccination rate in our group; however, 10.4% of our group was documented as having received the influenza virus vaccine and 3.8% received regular (annual) vaccinations. In hyposplenic cases, triple vaccination was documented in only 0.9%. Regarding pain-relieving medications, 51.9% of the group was given narcotics and 61.8% of these were chronic users. A total of 10.9% of patients receiving narcotics were reported to be dependent on narcotic medications. Nonsteroidal anti-inflammatory drugs were given to 86.8% of patients. The compliance is defined as complete adherence to the medications rather than erratic use of medications [Table 3].
The number of complications was used to measure the severity of the disease. Several factors that were considered significantly affect both the severity and course of the disease. Male gender correlated with increased severity, 67.3% of males (35 patients) had three or more complications compared to 32.7% of females (17 patients) who had three or more complications (P = 0.018). Another significant factor was area of origin; 84.2% of patients (32 patients) who were born in the Western and Southwestern areas had three or more complications. However, only 15.8% (6 patients) of those born in the Northern, Eastern, and Central areas had three or more complications (P = 0.007). Patients with positive family history have shown increased disease severity, with 90% (27 patients) of those with positive family history having three or more complications and 10% (3 patients) with no family history having three or more complications (P = 0.009) [Table 4].
|Table 4: Univariate analysis: Factors affecting severity outcome of the sickler patients|
Click here to view
| Discussion|| |
Demographic data has been shown to significantly influence the course of the disease. As indicated in the results, male patients were shown to have a higher incidence than female patients in our sample and male gender was associated with a more severe disease course. In addition, a study performed in Eastern Saudi Arabia reported that males have higher disease severity compared to females. Our results are consistent with studies reporting that SCA in males takes a more severe course compared to that in females.,, Individuals diagnosed with SCA from specific areas in Saudi Arabia, such as the Western and Southwestern provinces, have a higher incidence of complications and disease severity. The genotype of SCA in these areas correlated with the Benin-African genotype, which is known to be associated with a more severe disease phenotype compared with the Indian-Arab genotype, which is typically seen in patients from the Eastern region. Our study has shown that the predominant subtype is the SS type, which is associated with a higher rate of complications. In addition, a previous study reported that certain phenotypes such as the SS type had higher complication rates. In our study, it was not possible to assess or compare the different subtypes of SCA, as the predominant subtype in our patients was SS.
The majority of our patients presented with an acute painful crisis as an initial manifestation. Many studies worldwide have reported findings similar to those in our study; common reported manifestations include mild-to-severe anemia, painful crises, frequent infections, hand and foot syndrome, and stroke.,,,, This might be because the sample included patients with an SS type. The rate of other complications in our patient subgroup was similar to what has been reported in other studies, with minor differences. In comparison, stroke was seen in <2% of our group, while it is expected to be found in 10% of SCA patients in general.,, This could be due to the small sample size, the fact that the majority of patients in our group are adults and our inclusion of only a hospital-based patient cohort rather than a community cohort.
Our study has shown the average number of hospital admissions due to complications; VOC was the most common complication, a finding that was consistent with many studies globally.,,, A study performed in 2012 had findings similar to ours that 95% of their sample experienced a vaso-occlusive complication that required admission and they considered this “a hallmark” of the disease. The study also demonstrated that acute chest syndrome came after the VOC as a common complication. This same study demonstrated that 50% of cases occurred after the hospital admission for acute painful crisis. This might be because patients who are admitted are more susceptible to infections. Another study conducted in 1997 showed that the most common age group affected was children. This might be due to the maturity of the immune system of adults since children have immature immune systems.
We have studied AVN as a complication of Sickle cell anemia, specifically the number of joint involved and whether the patient had undergone joint replacement surgery. The study that was performed in 2012 also discussed AVN as a complication, especially the epiphyseal bones of the hip, shoulder, and spine; however, any joint could be affected. The prevalence was 26% in children and 48.6% in adults. The occurrence of AVN might be due to recurrent episodes of VOC since pain crises could cause infarcts and necrotization of the bones and with time could lead to damage in the bone marrow.
Hydroxyurea can be considered the standard of care and ideal agent for treating SCA as it provides multiple therapeutic benefits.,,,, We have also studied the efficacy of hydroxyurea treatment on hospital admissions due to SCD complications, before starting hydroxyurea, the average admission was five admissions in an average for 3 years, after initiating hydroxyurea, the average admission was three admissions in an average of 3 years. A study was published in November 2016 that included a group of pediatric age showed a decrease in hospital admissions, pain incidence, and emergency department visits due to complications. Our study discussed only the adult group, which may show different percentages since age could play a role in the efficacy of the treatment. A study conducted in 2014 showed that women with SCA had a higher rate of complications than those in the general population. The hemoglobin SS type also correlated with much worse complications than those in the hemoglobin SC type.
| Conclusion|| |
Although our study included a small sample and was performed at a single center, it showed that our patient group has clinical features and complications that are similar to those in previously reported studies. We found that the following three factors correlate with disease severity: Patient gender, region of origin, and family history of severe disease. The retrospective nature of the study may limit the accuracy of some of the data and more extensive studies are needed at a larger scale. These data need to be confirmed in a larger prospective or registry-based study.
The authors would like to acknowledge the help of Nature Editing Services for reviewing the manuscript and necessary editing for English grammar.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Azar S, Wong TE. Sickle cell disease: A Brief update. Med Clin North Am 2017;101:375-93.
Rees DC, Williams TN, Gladwin MT. Sickle-cell disease. Lancet 2010;376:2018-31.
Pauling L, Itano HA. Sickle cell anemia a molecular disease. Science 1949;110:543-8.
Elion J, Laurance S, Lapouméroulie C. Pathophysiology of sickle cell disease. Med Trop (Mars) 2010;70:454-8.
Powars DR, Chan LS, Hiti A, Ramicone E, Johnson C. Outcome of sickle cell anemia: A 4-decade observational study of 1056 patients. Medicine (Baltimore) 2005;84:363-76.
Ganguly A, Boswell W, Aniq H. Musculoskeletal manifestations of sickle cell anaemia: A pictorial review. Anemia 2011;2011:794283.
Steinberg MH. Sickle cell anemia, the first molecular disease: Overview of molecular etiology, pathophysiology, and therapeutic approaches. ScientificWorldJournal 2008;8:1295-324.
Awwalu S, Mamman AI, Hassan A, Dogara LG, Waziri AD, Aminu SM,et al
. Variations in the β-globin genes of sickle cell anaemia patients in Zaria, Northwestern, Nigeria. Niger J Clin Pract 2017;20:464-9.
] [Full text]
Nash GB, Johnson CS, Meiselman HJ. Mechanical properties of oxygenated red blood cells in sickle cell (HbSS) disease. Blood 1984;63:73-82.
Lonergan GJ, Cline DB, Abbondanzo SL. Sickle cell anemia. Radiographics 2001;21:971-94.
Ndefo UA, Maxwell AE, Nguyen H, Chiobi TL. Pharmacological management of sickle cell disease. Pharm Ther 2008;33:238-43.
Gravitz L, Pincock S. Sickle-cell disease. Nature. 2014;515(7526):S1.
Grosse SD, Odame I, Atrash HK, Amendah DD, Piel FB, Williams TN,et al
. Sickle cell disease in Africa: A neglected cause of early childhood mortality. Am J Prev Med 2011;41:S398-405.
Taiwo IA, Oloyede OA, Dosumu AO. Frequency of sickle cell genotype among the yorubas in lagos: Implications for the level of awareness and genetic counseling for sickle cell disease in Nigeria. J Community Genet 2011;2:13-8.
Makani J, Ofori-Acquah SF, Nnodu O, Wonkam A, Ohene-Frempong K. Sickle cell disease: New opportunities and challenges in Africa. ScientificWorldJournal 2013;2013:193252.
Lukusa Kazadi A, Ngiyulu RM, Gini-Ehungu JL, Mbuyi-Muamba JM, Aloni MN. Factors associated with growth retardation in children suffering from sickle cell anemia:First report from central Africa. Anemia 2017;2017:7916348.
Jastaniah W. Epidemiology of sickle cell disease in Saudi Arabia. Ann Saudi Med 2011;31:289-93.
] [Full text]
Alsultan A, Aleem A, Ghabbour H, AlGahtani FH, Al-Shehri A, Osman ME,et al
. Sickle cell disease subphenotypes in patients from Southwestern province of Saudi Arabia. J Pediatr Hematol Oncol 2012;34:79-84.
Alsultan A, Jastaniah W, Al Afghani S, Al Bagshi MH, Nasserullah Z, Al-Suliman AM,et al
. Demands and challenges for patients with sickle-cell disease requiring hematopoietic stem cell transplantation in Saudi Arabia. Pediatr Transplant 2016;20:831-5.
Udezue E, Girshab AM. Differences between males and females in adult sickle cell pain crisis in Eastern Saudi Arabia. Ann Saudi Med 2004;24:179-82.
Platt OS, Brambilla DJ, Rosse WF, Milner PF, Castro O, Steinberg MH,et al
. Mortality in sickle cell disease. Life expectancy and risk factors for early death. N
Engl J Med 1994;330:1639-44.
Adekile AD, Huisman TH. Level of fetal hemoglobin in children with sickle cell anemia: Influence of gender, haplotype and alpha-thalassemia-2 trait. Acta Haematol 1993;90:34-8.
Rami Helvaci M, Ayyildiz O, Gundogdu M. Gender differences in severity of sickle cell diseases in non-smokers. Pak J Med Sci 2013;29:1050-4.
El-Hazmi MA, Al-Hazmi AM, Warsy AS. Sickle cell disease in middle East Arab countries. Indian J Med Res 2011;134:597-610.
] [Full text]
Kavanagh PL, Sprinz PG, Vinci SR, Bauchner H, Wang CJ. Management of children with sickle cell disease: A comprehensive review of the literature. Pediatrics 2011;128:e1552-74.
Diagne I, Diagne-Gueye ND, Signate-Sy H, Camara B, Lopez-Sall P, Diack-Mbaye A,et al
. Management of children with sickle cell disease in Africa: Experience in a cohort of children at the royal albert hospital in dakar. Med Trop (Mars) 2003;63:513-20.
Lê PQ, Ferster A, Cotton F, Vertongen F, Vermylen C, Vanderfaeillie A,et al
. Sickle cell disease from Africa to belgium, from neonatal screening to clinical management. Med Trop (Mars) 2010;70:467-70.
Babela JR, Nzingoula S, Senga P. Sickle-cell crisis in the child and teenager in Brazzaville, Congo. A retrospective study of 587 cases. Bull Soc Pathol Exot 2005;98:365-70.
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.
Njamnshi AK, Mbong EN, Wonkam A, Ongolo-Zogo P, Djientcheu VD, Sunjoh FL,et al
. The epidemiology of stroke in sickle cell patients in Yaounde, Cameroon. J Neurol Sci 2006;250:79-84.
Kassim AA, Galadanci NA, Pruthi S, DeBaun MR. How I treat and manage strokes in sickle cell disease. Blood 2015;125:3401-10.
Salman ZA, Hassan MK. Hospitalization events among children and adolescents with sickle cell disease in Basra, Iraq. Anemia 2015;2015:195469.
Loureiro MM, Rozenfeld S. Epidemiology of sickle cell disease hospital admissions in Brazil. Rev Saude Publica 2005;39:943-9.
Aljuburi G, Laverty AA, Green SA, Phekoo KJ, Banarsee R, Okoye NV,et al
. Trends in hospital admissions for sickle cell disease in England, 2001/02-2009/10. J Public Health (Oxf) 2012;34:570-6.
Ikefuna AN, Emodi IJ. Hospital admission of patients with sickle cell anaemia pattern and outcome in Enugu area of Nigeria. Niger J Clin Pract 2007;10:24-9.
] [Full text]
Ballas SK, Kesen MR, Goldberg MF, Lutty GA, Dampier C, Osunkwo I,et al
. Beyond the definitions of the phenotypic complications of sickle cell disease: An update on management. ScientificWorldJournal 2012;2012:949535.
Quarmyne MO, Dong W, Theodore R, Anand S, Barry V, Adisa O,et al
. Hydroxyurea effectiveness in children and adolescents with sickle cell anemia: A large retrospective, population-based cohort. Am J Hematol 2017;92:77-81.
Hounkpe BW, Fiusa MM, Colella MP, da Costa LN, Benatti Rde O, Saad ST,et al
. Role of innate immunity-triggered pathways in the pathogenesis of sickle cell disease: A meta-analysis of gene expression studies. Sci Rep 2015;5:17822.
Vaishya R, Agarwal AK, Edomwonyi EO, Vijay V. Musculoskeletal manifestations of sickle cell disease: A Review. Cureus 2015;7:e358.
Lanzkron S, Strouse JJ, Wilson R, Beach MC, Haywood C, Park H,et al
. Systematic review: Hydroxyurea for the treatment of adults with sickle cell disease. Ann Intern Med 2008;148:939-55.
Agrawal RK, Patel RK, Shah V, Nainiwal L, Trivedi B. Hydroxyurea in sickle cell disease: Drug review. Indian J Hematol Blood Transfus 2014;30:91-6.
McGann PT, Ware RE. Hydroxyurea therapy for sickle cell anemia. Expert Opin Drug Saf 2015;14:1749-58.
Singh A, Xu YJ. The cell killing mechanisms of hydroxyurea. Genes (Basel) 2016;7. pii: E99.
Pule GD, Mowla S, Novitzky N, Wonkam A. Hydroxyurea down-regulates BCL11A, KLF-1 and MYB through miRNA-mediated actions to induce γ-globin expression: Implications for new therapeutic approaches of sickle cell disease. Clin Transl Med 2016;5:15.
Oteng-Ntim E, Meeks D, Seed PT, Webster L, Howard J, Doyle P,et al
. Adverse maternal and perinatal outcomes in pregnant women with sickle cell disease: Systematic review and meta-analysis. Blood 2015;125:3316-25.
[Table 1], [Table 2], [Table 3], [Table 4]
|This article has been cited by|
||The Correlation Between Surgical Procedures and Quality of Life Among Sickle Cell Disease Patients: A Perspective Saudi Study
| ||Ali J Al Saad, Rayan A Buhalim, Faisal A Al Jabr, Abdulaziz M Al Dehailan, Abdulaziz A Albahrani |
| ||Cureus. 2022; |
|[Pubmed] | [DOI]|
||Reasons for Hospitalization of Sickle Cell Disease Patients in the Eastern Province of Saudi Arabia: A Single-Center Study
| ||Ossama M Zakaria, Rayan A Buhalim, Faisal A Al Jabr, Mohammed N AlSaeed, Ibrahim A Al-Hajji, Yousif A Al Saleh, Mohammed A Buhalim, Abdulaziz M Al Dehailan |
| ||Cureus. 2021; |
|[Pubmed] | [DOI]|
||Paediatric sickle cell disease at a tertiary hospital in Malawi: a retrospective cross-sectional study
| ||Chikondi Sharon Chimbatata,Master RO Chisale,Alfred Bornwell Kayira,Frank Watson Sinyiza,Balwani Chingatichifwe Mbakaya,Paul Uchizi Kaseka,Pocha Kamudumuli,Tsung-Shu Joseph Wu |
| ||BMJ Paediatrics Open. 2021; 5(1): e001097 |
|[Pubmed] | [DOI]|
||Analysis of Causes of Hospitalization Among Children with Sickle Cell Disease in a Group of Private Hospitals in Jeddah, Saudi Arabia
| ||Shereen M Abd El-Ghany,Aisha T Tabbakh,Khulud I Nur,Rayan Y Abdelrahman,Sara M Etarji,Bayan Y Almuzaini |
| ||Journal of Blood Medicine. 2021; Volume 12: 733 |
|[Pubmed] | [DOI]|
||Sickle cell avascular necrosis: Prevalence and clinical profiles in a tertiary hospital northwestern Nigeria
| ||Sani Awwalu,Abdulaziz Hassan,Ibrahim U. Kusfa,Aliyu D. Waziri,Ismaila N. Ibrahim,Garba Yahaya |
| ||Annals of African Medical Research. 2020; 3(1) |
|[Pubmed] | [DOI]|