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Evaluation of the Lipid Profile in Patients with�Thalassemia�Major in South Khorasan Province, Iran
Tayyebeh Chahkandi, M.D. 1, Nahid Azdaki, M.D. 2,*, Mansoureh Baradaran, M.D. 3, and Reyhane Hoshyar, Ph.D. 4,*
 
1Department of Pediatric; 2Cardiovascular Diseases Research Center, Department of Cardiology; 3Student Research Committee; 4Cellular & Molecular Research Center, Department of Clinical Biochemistry, Medicine School, Birjand University of Medical Sciences, Birjand, Iran


*Corresponding authors: Dr Reyhane Hoshyar, Cellular & Molecular Research Center, Birjand University of Medical Sciences, Birjand, Iran. 
Tel: +98-56-32381542
Fax: +98-56-32430076
Email:  HYPERLINK "mailto:reyhaneh.houshyar@gmail.com" reyhaneh.houshyar@gmail.com
Dr Nahid Azdaki, Cardiovascular Diseases Research Center, Birjand University of Medical Sciences Birjand, Iran. Email: HYPERLINK "mailto:nahidazdaki@yahoo.com"nahidazdaki@yahoo.com 


















Abstract
Thalassemia Major is a disease accompanied by changes in the lipid levels and oxidative stress conditions which can lead to cardiac complications and early death. This study aimed to evaluate the lipid profile in these patients. In this case-control study the serum levels of lipids including cholesterol, triglycerides (TG), HDL and LDL were measured in 48 patients with thalassemia major (25 male and 23 female patients) with a mean age of 13.2�6.6 years and 48 healthy people, and after age and sex matching, their relation with the amount of ferritin, hemoglobin, and such parameters as age, sex, weight and height were analyzed.  Compared with the healthy subjects, the patients with thalassemia major had higher plasma levels of TG (P<0.005) and (TC P<0.005) lower HDL levels (P<0.005). Plasma levels of LDL were also lower in the patients group than the control group, but this difference was not statistically significant (P<0.21). The average lipid level had no significant relationship with age, sex, weight and height. The comparison of lipids level for average hemoglobin amounts was only significant for TC and HDL (P=0.007). In addition, there was no significant relationship between lipids and ferritin in the patients (P =0.367). Regular and heavy use of effective chelators for reducing the iron loads, as well as performing periodic lipid profile tests can play a great role in preventing from cardiovascular diseases caused by the changes in lipid profile and therefore in decreasing the rate of death in patients with thalassemia major.
Keywords:��-Thalassemia Major; Lipid Profile; Birjand














Introduction
Thalassemia is the most common monogenic disorder around the world, including Iran [1], which involves a quantitative defect in glob in chain production [2]. Annually, about sixty thousand infants are born with severe forms of the disease [3]. Survival in patients with thalassemia majors dependent on lifelong blood transfusion [4,5]. Iron overload and increased ferritin levels due to frequent transfusions will lead to increased oxidative stress conditions and lipid peroxidation and consequently the change in the lipid profile [6]. Several studies report the existence of abnormal lipid profiles in patients with thalassemia. This dyslipidemia includes high triglycerides, low Total Cholesterol (TC), low HDLand high TC to HDL ratio in such patients [7]. Lower HDL level in these patients is a risk factor for coronary artery diseases. Recent studies suggest that children with thalassemia major are at risk of subclinical atherosclerosis [8], and also that a relationship has been proved between dyslipidemia and early atherosclerosis in these patients [7]. There has proved to bea direct relationship between carotid thickness, which is a factor for measuring atherosclerosis, and the age, serum ferritin level and cholesterol level [9].
This study aimed to study the lipid profiles including TC, TG, LDL and HDL in patients with thalassemia major and to evaluate the relationship between these profiles and ferritin, hemoglobin and also such parameters as age, sex, weight and height.

Methods
Study population
This case-control study studied 48 patients with thalassemia major referring to Special Diseases Clinic of Birjand, eastern Iran (25 male and 23 female patients) with a mean age of 13.2�6.6 years and 48 healthy people. Both groups were completely matched for age and sex. After explaining the objectives and taking the subjects� consent, the medical history and physical examinations were performed including measurements of height and weight. 
Clinical and demographic characteristics
Following 12 hours of fasting, blood samples were taken from the subjects and were sent to the laboratory in order to measure the cholesterol, triglycerides, HDL and LDL levels. The obtained blood samples were then centrifuged and analyzed using a biochemical auto-analyzer (Prestige 24I, made in Japan). In this study, the NHLBI (2011) diagnostic panel was utilized for diagnosis of lipid disorders. In this panel, the acceptable, borderline and abnormal indices are defined as follows:
Borderline: HDL<45 mg/dl, LDLe"100 mg/dl, TCe"170 mg/dl and TG>130 mg/dl;
Abnormal: HDL<35 mg/dl, LDLe"130 mg/dl, TCe"200 mg/dl and TG>130 mg/dl. 
The rates of ferritin and hemoglobin were also extracted from the information contained in the files. In addition, the exclusion criteria in this study were diabetes mellitus, hepatitis B and C, liver and kidney disease and taking any medication affecting serum lipid levels.
Ethical considerations 
Personal identity of patients was confidentially recorded in questionnaires and only analysis of results was reported. Moreover, the researchers regarded all contents of the the Research Council and Ethics of Birjand University of Medical Sciences throughout the study.
Statistical analysis
The data were collected, coded and entered into SPSS software (version 22). In order to provide descriptive statistical information, the frequency tables, diagrams, measures of central tendency and dispersion, mean, standard deviation and Pearson correlation test were utilized. The independent T-test was used for the comparison of means of the two groups, and in case of non-normal distribution, the Mann Whitney test was utilized.
Results
In the present study, 48 patients with �-thalassemia major and 48 healthy controls, (including 25 male (52.1%) and 23 female (47.9%) patients) with a mean age of 13.2�6.6 years were studied. Both groups were completely matched for age and sex. Compared with the healthy subjects, the patients with thalassemia major had lower plasma levels of TC and HDL and higher levels of TG (P<0.005). Plasma levels of LDL were also lower in the patients group than the control group, but this difference was not statistically significant (P=0.21) (Table 1). About 87.5% of the subjects in the thalassemia group showed abnormal HDL index which suggests a statistically significant difference.



Table 1.�Comparison of Mean Lipid Profile in Female Patients with Thalassemia Major and the Control Group
LDL
(mg/dl)HDL
(mg/dl)TG
(mg/dl)TC
(mg/dl)Group1.04070.708�35.55430.06�11.41118.6�58.05123.2�31.6MT*1.07278.125�20.302644.97�11.9179.7�53.79148.8�24.3ControlP<0.21P<0.005P<0.005P<0.005Significance47=df
t= 1.13df = 47
t = 6.63df = 47
t = 4.53
df = 47
t = 4.53
Paired T-test Results
*MT:�Major�Thalassemia,�TG: Triglycerides,�TC:�Total�Cholesterol,�HDL:High-Density�Lipoprotein,�LDL: Low-Density Lipoprotein
Using Pearson correlation analysis it was revealed that the average lipid values had no significant relationship with sex, age, weight and height parameters. Analysis of the lipids on the basis of the sex showed that the mean values of all types of lipids in the thalassemia group were higher in the female sex (P=0.606). The age in the thalassemia group had an impact on cholesterol, HDL and LDL, but it had no impact on any of the variables in the control group. Analysis of the lipids on the basis of the age showed that the mean values of the lipids in the thalassemia group were the highest in the range of 3-11 years of age, and after that, the increase in age lead to the increase in the lipids level, except TG. But in the control group, the age range of19-27 had the maximum mean amounts of lipids. The age had a positive and direct relationship with cholesterol, HDL and LDL variables, but a reverse relationship with triglyceride. There was no significant relationship between the lipids and the patients� age (P=0.123).The relationship between the BMI in thalassemia major patients with ferritin and hemoglobin was analyzed using Pearson correlation analysis. The results showed that there was no significant relationship between the patients� BMI and the mentioned factors (Table 2).
Table 2. The�Relationship between�BMI�and Ferritin and Hemoglobin in Patients with Thalassemia Major Based on Pearson Correlation Analysis
Clinical/Laboratory DataPearson r Test ResultP ValueFerritin-0.150.29HB0.040.78

The relationship between the lipids (cholesterol, TG, LDL and HDL) was studied by the use of one-way ANOVA and the results showed that due to the significance level of the relationship between BMI and any of the cholesterol, triglycerides, LDL and HDL lipids which respectively amounted to 0.692, 0.067, 0.078 and 0.573, it can be said that there is no significant relationship between the BMI and any of the lipids. In addition, the relationship between the BMI and the lipids was studied using Pearson correlation analysis, and according to the results in table 3, no significant relationship was observed between the BMI and the lipid profile in patients with thalassemia major. The weight had a positive and direct relationship with cholesterol and LDL variables, but a reverse relationship with triglyceride and HDL. There was no significant relationship between the lipids and the patients� weight (P=0.056). The height had a negative and reverse relationship with cholesterol, LDL and HDL variables, but only a direct relationship with triglyceride. There was no significant relationship between the lipids and the patients� height (P=0.643). Ferritin had a positive and direct relationship with cholesterol, triglyceride and LDL variables, but a reverse relationship with HDL. There was no significant relationship between the lipids and ferritin (P=0.367).
Table 3.�The Relationship between�BMI�and Lipid Profiles in Patients with Thalassemia Major Based on Pearson Correlation Analysis
Clinical/Laboratory dataPearson r Test ResultP ValueTG-0.1732 to 0.38800.4295TC-0.4285 to 0.12580.2646HDL-0.4264 to 0.12820.2717LDL-0.3935 to 0.16690.4045
The maximum and minimum average amounts of TC, HDL and LDL in patients with thalassemia, were respectively in the average hemoglobin amounts of (8.9 - 8.10 gr/dl) and (1.7 - 8 gr/dl). The maximum and minimum average range of TG in the thalassemia group, were respectively in the average hemoglobin range of (1.7 - 8 gr/dl) and (8.9 - 8.10 gr/dl). The average rate of hemoglobin had a positive and direct relationship with cholesterol, HDL and LDL variables, but a reverse relationship with triglyceride. Comparison of the lipid levels on the basis of the average hemoglobin amount was only significant for TC and HDL (P=0.007).
Discussion 
Thalassemia Major is a disease accompanied by changes in the lipid levels and oxidative stress conditions which can lead to cardiac complications and early death [10]. The results of this study revealed a decrease in the plasma levels of HDL and TC in patients with thalassemia compared to the healthy subjects (P<0.001). However, the plasma concentration of TG was higher than the healthy subjects (P<0.001). The amount of LDL was lower in the thalassemia patients than the control group, which was not statistically significant (P<0.21). These results were consistent with the findings of many researchers [11,12]. A study was carried out by Madani in western Iran, in which kidney lipid levels in patients with thalassemia were reported to be lower than the control group, however, the thalassemia group had higher TG levels than the control group [9]. Absalan conducted a study in Yazd Blood Transfusion Centerand reported that the TC-HDL-LDL levels in patients with thalassemia were lower than the control group [13]. In another study by Bordbar et al. in northern Iran, the TC and LDL levelsin patients with thalassemia were reported to be lower than the control group [14]. In addition, in another study by Ferdaus et al. in Bangladesh, the majority of patients with thalassemia had normal lipid levels; however, the HDL level was lower in patients with thalassemia than the control group [11]. A study of the serum levels of lipids and lipoproteins in Syrian patients with beta-thalassemia major suggested that with the exception of TG, thalassemia patients generally had lower lipid profiles [15]. Results of a study by Gurselet al. in Ankara also showed a significant decrease in the rate of HDL, LDL and TG in patients with beta thalassemia compared to the control group [16]. 
The anemia-related plasma hemo-dilution, increased cholesterol consumption due to erythroid hyperplasia, macrophage activation with cytokine release, and liver damage secondary to iron overload will justify the decrease in the cholesterol levels of the patients with thalassemia. Lower level of LDL is also secondary to the increase in the removal by macrophage [17]. The increased TG level in thalassemic patients is probably caused by the decrease in the lipolytic activity secondary to liver diseases [12]. Most papers have suggested that the reason for the increase in TG and the decrease in other lipids is the oxidative damage effect and lipid peroxidation inpatients with thalassemia [18]. More specifically it can be asserted that decreased activity of such enzymes as LP-PLA2 as a result of oxidative damage may justify lipid profile disorders [19].
The average lipid amounts had no significant relationship with gender and age. In a study by Livrea et al. in Italy, no relationship was observed between the patients� age and LDL plasma level [20]. In a study by Bordbar et al. in northern Iran, a direct relationship was observed between the TC levels and the increase in age [14].A study by Dr. Nasr et al. in Egypt found no correlation between the lipid plasma levels and the age, but a direct correlation between the LDL to HDL ratio and the age [17].Another research was conducted by Tantawy et al. in Egypt which studied the subclinical atherosclerosis in young �-thalassemia major patients, and suggested that there was a direct relationship between carotidintimal-medialthickness and the age [21].
In the present study no significant relationship was observed between the average lipid amounts and the thalassemic patients�height and weight, but this may have been caused by various factors including the limitations of the statistical population. This study also revealed in patients with thalassemia, the increase in ferritin level will lead to the increase in LDL and TG levels and a decrease in HDL level which was not statistically significant (p=0.367). The study by Bordbar in northern Iran on the patients with thalassemia major and intermedia revealed a direct relationship between ferritin serum level and the levels of TG, TC and LDL [14]. Dr. Nasr et al. found no correlation between plasma levels of lipids and the ferritin level [17]. The study by Tantawyet al. suggested that there was a direct relationship between carotid intimal-medialthickness and the ferritin level [21]. The reason for the change in the lipid profile with the increase in ferritin can be the oxidative damage caused by iron overload [15]. In a study by Sengsuk in India, the relationship between ferritin and lipid profile was significant [6].
The study by Bordbar in northernIran on the patients with thalassemia reported a direct relationship betweenlipid levels and hemoglobin concentration in thalassemia major patients.14 In their study in Egypt, Dr. Nasr et al. found no correlation between lipid levels and hemoglobin level [17]. The increased blood transfusion and consequently iron overload and the subsequent increase in oxidative damages may justify the change in lipid profiles by the increase in hemoglobin [22].
The limitation of our study was the small sample size and therefore the results may not be successfully generalized to all patients with thalassemia. The process of lipid oxidation and atherogenesis as a result of iron overload in patients with thalassemia as well as the changes in the lipid profile and the decrease in HDL secondary to the increase in ferritin can increase the risk of coronary diseases and early death in these patients. Regular and heavy use of effective chelators for reducing the iron loads are suggested for preventing from cardiovascular diseases caused by the changes in the lipid profile. On the other hand, performing periodic lipid profile tests can play a great role in increasing the longevity and decreasing the rate of death in patients with thalassemia major.
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