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Surrogates of Pulmonary Arterial Hypertension (PAH) in Adult Patients with Homozygous Sickle Cell Disease in Bahrain: An Echocardiographic Study.



Taysir Garadah,  FRCP 1, 2;  Adla  B. Hassan  MD,1,2   Mohamed  AlAlawi , MD1; Ahmed Jaradat, PhD, 2  Reginald Sequeira,  PhD2   Fathia Qureshi1  

1 Salmaniya Medical Complex, Ministry of Health, Manama, Kingdom of Bahrain.
2 College  of Medicine and Medical Sciences, Arabian Gulf University, Manama, Kingdom of Bahrain.






Address for correspondence:
Dr. Taysir Garadah
P.O. Box 18725
Manama, Kingdom of Bahrain
E mail: HYPERLINK "mailto:garadaht@hotmail.com"garadaht@hotmail.com
Tel; 00973 17239681
Fax 00973 17230730



ABSTRACT
Background: Pulmonary Arterial hypertension (PAH) is a late complication in adult patients with homozygous sickle cell disease (SCD). The early identification of PAH may be of paramount importance.
Aim: 1-To study the correlation between serum level of NT pro BNP hormone, ferritin and PAH in adult patients with SCD . 2- Evaluate the predictive risk of pulsed and tissue Doppler variables of echocardiogram for the development of PAH in SCD.
Method: In this cross sectional prospective study,103 patients with homozygous SCD were studied and compared with aged and gender matched healthy control. Every patient had a clinical assessment, pulsed and tissue Doppler evaluation. Blood samples were withdrawn for the level of haemoglobin, ferritin and NT pro BNP hormone. The mean difference between the two groups for echo Doppler and biometric variables were assessed.  Multiple regression analysis applied for measuring the odds ratio of different biometric and Doppler variables for risk of PAH in SCD.
Results:  The study group  consist of  103 patients with SCD, mean age of 28.52� 14.11 year, (range 14-42), with 68 male (66.0 %).  Patients with SCD compared with control had a significantly low diastolic pressure, lower haemoglobin level and but high serum level ferritin and pro BNP hormone. Further, there was a significant increment in the left atrium area (LA), higher right ventricle (RV) wall thickness and diameter. The RV tricuspid annular systolic excursion (TAPSE) was high of 1.42�0.21 vs. 1.11�0.23, P<0.05. RV pulsed Doppler data showed restrictive filling pattern with significant higher E wave velocity, high E/A ratio and short DT. Further, the ratio of upper pulmonary vein for systolic /diastolic Doppler velocity was significantly lower 1.5 �0.12 vs. 2.4�0.11, p<0.05. The tissue Doppler of lateral annulus of tricuspid valve in SCD patients  showed a significantly lower S wave of 6.7 � 1.7 vs 11.3� 1.9 ,p<0.01, higher E/E- ratio and lower A-wave. The incidence of pulmonary hypertension in SCD patients via tricuspid valve velocity defined as e"2.5 m/s was 33%. There were positive correlation between the serum level of ferritin, NT pro BNP hormone and tricuspid valve velocity of (r= 0.38) and (r=0.43) respectively. The odds ratio for development of PAH was 3.1 for E/E- ratio e"13,  2.5 for DT of <160 msec, 2.2 for LVMI >121 gm/M2, , 1.9 for ferritin e"600 (g/l , 1.6 cm for left atrial area e"20 cm, 1.3 for pro- BNP e" 150 Pmol/L.
Conclusion: Adult patients with SCD have normal LV systolic function but RV diastolic dysfunction suggestive of restrictive pattern. Thirty three percent had pulmonary hypertension with positive correlation between both serum levels of ferritin, NT pro BNP hormone. The risk of PAH in SCD patients is higher if the shorter DT <160 msec, LVMI >121 gm/M2, left atrial area e"20 cm, E/E- ratio e" 13 and RV wall thickness >3 mm.



KEY WORDS: Adult Sickle cell disease, Tissue Doppler echocardiogram, pro-BNP, Bahrain
Introduction
Sickle cell anaemia (SCA) is a form of hereditary haemolytic anaemia characterized by the synthesis of an abnormal haemoglobin S.  It is  caused by the substitution of amino acid valine for glutamic acid at position six of the globin chain of haemoglobin leading to an abnormal mutant haemoglobin HbS in its homozygous form (HbSS)  ADDIN EN.CITE <EndNote><Cite><Author>Bunn</Author><Year>1997</Year><RecNum>5</RecNum><DisplayText>[1]</DisplayText><record><rec-number>5</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">5</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Bunn, H. F.</author></authors></contributors><auth-address>Division of Hematology, Brigham and Women&apos;s Hospital, Harvard Medical School, Boston, MA 02115, USA.</auth-address><titles><title>Pathogenesis and treatment of sickle cell disease</title><secondary-title>N Engl J Med</secondary-title><alt-title>The New England journal of medicine</alt-title></titles><periodical><full-title>N Engl J Med</full-title><abbr-1>The New England journal of medicine</abbr-1></periodical><alt-periodical><full-title>N Engl J Med</full-title><abbr-1>The New England journal of medicine</abbr-1></alt-periodical><pages>762-9</pages><volume>337</volume><number>11</number><edition>1997/09/11</edition><keywords><keyword>Anemia, Sickle Cell/etiology/*physiopathology/*therapy</keyword><keyword>Antisickling Agents/therapeutic use</keyword><keyword>Fetal Hemoglobin</keyword><keyword>Hemoglobin, Sickle/chemistry</keyword><keyword>Humans</keyword><keyword>Hydroxyurea/therapeutic use</keyword></keywords><dates><year>1997</year><pub-dates><date>Sep 11</date></pub-dates></dates><isbn>0028-4793 (Print)&#xD;0028-4793 (Linking)</isbn><accession-num>9287233</accession-num><work-type>Review</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/9287233</url></related-urls></urls><electronic-resource-num>10.1056/NEJM199709113371107</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_1" \o "Bunn, 1997 #5" 1].  Patients usually presented with various clinical manifestations such as vaso-occlusive crisis, recurrent haemolytic anaemia with the entrapment of red blood corpuscle in the microvasculature system leading to multi organ infraction that cause an organ dysfunction  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_2" \o "Platt, 1994 #6" 2].
The term sickle cell disease (SCD) denotes a pathological condition that can lead to severe complications or death. Sickle-cell disease occurs more among patients whose ancestors lived in tropical and sub-tropical regions where malaria is common.  The incidence of SCD in the Saudi Arabian peninsula is in the range of 1.2% to 2.6%  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_3" \o "Alhamdan, 2007 #8" 3,  HYPERLINK \l "_ENREF_4" \o "Nasserullah, 2003 #9" 4].  SCD patient had a variety of cardiac manifestations depending on the methods of evaluation and the study population according to ethnicity and geographical distribution  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_5" \o "el-Hazmi, 1996 #10" 5,  HYPERLINK \l "_ENREF_6" \o "Pearson, 1999 #11" 6].  In homozygous SCD, the earliest marker of cardiac involvement is abnormal diastolic function followed by cardiomegaly and pulmonary hypertension in adulthood with or without heart failure  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_7" \o "Batra, 2002 #13" 7,  HYPERLINK \l "_ENREF_8" \o "Zilberman, 2007 #12" 8].
Pulse Doppler echocardiography is commonly used as a non-invasive tool for mitral and tricuspid flow for the pattern of LV diastolic filling  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_9" \o "Bahl, 1992 #14" 9,  HYPERLINK \l "_ENREF_10" \o "Lindqvist, 2009 #15" 10].  The LV diastolic filling pattern on pulsed Doppler has been classified into abnormal relaxation, pseudo-normal and restrictive pattern based on the ration of early diastolic filling velocity wave E to late filling velocity wave A.  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_11" \o "Choong, 1987 #16" 11]. The pattern of abnormal  relaxation pattern had low  early filling wave (E) , high atrial wave (A) with E/A ratio < 1  and prolonged deceleration time of E wave (DT)  The constrictive pattern had a  high E wave velocity, diminished or absent A wave with E/A ratio > 2 and shortened DT of <160 msec  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_12" \o "Nishimura, 1993 #83" 12,  HYPERLINK \l "_ENREF_13" \o "Ommen, 2000 #23" 13].  Tissue Doppler velocity of mitral and tricuspid valve annulus as well as pulmonary venous velocities, were validated as extra diagnostic tools for right and left ventricular diastolic dysfunction  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_14" \o "Ghaderian, 2012 #26" 14,  HYPERLINK \l "_ENREF_15" \o "Naqvi, 2001 #24" 15].
Pulmonary hypertension (PH) is a recognized complication in patients with SCD and beta thalassemia major  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_16" \o "Derchi, 1999 #27" 16,  HYPERLINK \l "_ENREF_17" \o "Sutton, 1994 #85" 17]. Several studies revealed a prevalence of 20-40% and that the presence of PAH is associated with high risk of mortality  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_18" \o "Ataga, 2004 #28" 18,  HYPERLINK \l "_ENREF_19" \o "Castro, 2003 #30" 19].
The NT-Pro B-type natriuretic peptide (pro BNP) is a hormone released in response to stretch of myocardial cell. The prognostic value of pro BNP has been demonstrated in several cardiovascular disorders  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_20" \o "Arad, 1996 #32" 20,  HYPERLINK \l "_ENREF_21" \o "Yap, 2004 #31" 21]. The level of pro BNP  has been shown to correlate with the severity of pulmonary hypertension and right ventricle dysfunction  ADDIN EN.CITE <EndNote><Cite><Author>Arad</Author><Year>1996</Year><RecNum>32</RecNum><DisplayText>[20]</DisplayText><record><rec-number>32</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">32</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Arad, M.</author><author>Elazar, E.</author><author>Shotan, A.</author><author>Klein, R.</author><author>Rabinowitz, B.</author></authors></contributors><auth-address>Heart Institute, Sheba Medical Center, Tel-Hashomer, Israel.</auth-address><titles><title>Brain and atrial natriuretic peptides in patients with ischemic heart disease with and without heart failure</title><secondary-title>Cardiology</secondary-title><alt-title>Cardiology</alt-title></titles><periodical><full-title>Cardiology</full-title><abbr-1>Cardiology</abbr-1></periodical><alt-periodical><full-title>Cardiology</full-title><abbr-1>Cardiology</abbr-1></alt-periodical><pages>12-7</pages><volume>87</volume><number>1</number><edition>1996/01/01</edition><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Analysis of Variance</keyword><keyword>Angina Pectoris/blood</keyword><keyword>Atrial Natriuretic Factor/*blood</keyword><keyword>Female</keyword><keyword>Heart Failure/*blood/etiology</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Myocardial Ischemia/*blood/complications</keyword><keyword>Natriuretic Peptide, Brain</keyword><keyword>Nerve Tissue Proteins/*blood</keyword><keyword>Prognosis</keyword><keyword>Radioimmunoassay</keyword><keyword>Regression Analysis</keyword><keyword>Sensitivity and Specificity</keyword></keywords><dates><year>1996</year><pub-dates><date>Jan-Feb</date></pub-dates></dates><isbn>0008-6312 (Print)&#xD;0008-6312 (Linking)</isbn><accession-num>8631038</accession-num><work-type>Comparative Study</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/8631038</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_20" \o "Arad, 1996 #32" 20]. The serum stable and the easily assayed NT-pro BNP have been shown useful in the stratification of pulmonary hypertension  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_22" \o "Souza, 2007 #34" 22]. 
The aims of the study is: 1- evaluates the usefulness of NT pro BNP in the assessment of diastolic function of RV in adult patients with sickle cell disease.2- Assess the predictive risk of serum level of NT pro BNP hormone and ferritin with other pulsed and tissue Doppler indices  for the development of pulmonary hypertension in patients with SCD.3- measure the usefulness of tissue Doppler velocity of lateral annulus of tricuspid valve in the assessment of diastolic function of RV in adult patients with SCD. 
Material and Methods 
Study population 
One hundred and three patients with sickle cell disease (SCD), with age of 14 to 42 year were enrolled in the study. The study was conducted over 12 months from end of sept 2012 to first of October 2013.  Patient selection was consecutive from those attending the haematology outpatient in Salmaniya Medical Complex (SMC). SMC is the main governmental hospital in the Kingdom of Bahrain with a catchment area of 900,000 populations.  The control group was 103 healthy patients matching for age and sex and they were referred to cardiology clinic for echocardiogram evaluation of a murmur or left ventricle function. Patients with sickle cell disease SCD and homozygous haemoglobin S (HbSS) were included. The diagnosis was based on haemoglobin electrophoresis and solubility screening test.  An informed consent obtained from the study patients. The study protocol was approved by the institutional committee.
Patients with SCD were excluded if they had haemo-globinopathy, history of blood transfusion within three weeks, adult congenital heart disease, hypertrophic cardiomyopathy, and advanced hepatic or renal failure. Patients� comprehensive history and clinical examination for blood pressure in mmHg and heart rate per min, presence of raised jugular venous pulse, heart murmur, crackles, S3 gallop, and ankle oedema were recorded.  Each patient gave a blood sample for the serum level of NT pro BNP, haemoglobin (HB) and ferritin.
Echocardiographic evaluation
Complete echocardiographic pulsed and tissue Doppler assessment was performed by Hew let Packard (e33) echo machine, using 2.5 MHz transducer by the same cardiologist.  The measurement of M mode, 2D, pulsed and tissue Doppler echocardiogram was performed by a single technician who is blinded of the clinical status and according to the American Society of Echocardiography guidelines  ADDIN EN.CITE <EndNote><Cite><Author>Sahn</Author><Year>1978</Year><RecNum>90</RecNum><DisplayText>[23]</DisplayText><record><rec-number>90</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">90</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Sahn, D. J.</author><author>DeMaria, A.</author><author>Kisslo, J.</author><author>Weyman, A.</author></authors></contributors><titles><title>Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements</title><secondary-title>Circulation</secondary-title><alt-title>Circulation</alt-title></titles><periodical><full-title>Circulation</full-title><abbr-1>Circulation</abbr-1></periodical><alt-periodical><full-title>Circulation</full-title><abbr-1>Circulation</abbr-1></alt-periodical><pages>1072-83</pages><volume>58</volume><number>6</number><edition>1978/12/01</edition><keywords><keyword>Aorta</keyword><keyword>Cardiac Volume</keyword><keyword>Diastole</keyword><keyword>Echocardiography/*standards</keyword><keyword>Electrocardiography</keyword><keyword>Heart Atria</keyword><keyword>Heart Septum</keyword><keyword>Heart Ventricles</keyword><keyword>Humans</keyword><keyword>Mitral Valve/physiology</keyword><keyword>Systole</keyword></keywords><dates><year>1978</year><pub-dates><date>Dec</date></pub-dates></dates><isbn>0009-7322 (Print)&#xD;0009-7322 (Linking)</isbn><accession-num>709763</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/709763</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_23" \o "Sahn, 1978 #90" 23]. The LV ejection fraction (EF percent) was assessed using the biplane Simpson methods  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_24" \o "Lang, 2005 #35" 24]. The M-mode guided echo was used to assess the systolic and end diastolic diameter of left ventricle cavity as well as the septum and posterior wall. The LV mass index was calculated as per formula described by Devereux et al. ADDIN EN.CITE <EndNote><Cite><Author>Devereux</Author><Year>1986</Year><RecNum>39</RecNum><DisplayText>[25]</DisplayText><record><rec-number>39</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">39</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Devereux, R. B.</author><author>Alonso, D. R.</author><author>Lutas, E. M.</author><author>Gottlieb, G. J.</author><author>Campo, E.</author><author>Sachs, I.</author><author>Reichek, N.</author></authors></contributors><titles><title>Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings</title><secondary-title>Am J Cardiol</secondary-title><alt-title>The American journal of cardiology</alt-title></titles><periodical><full-title>Am J Cardiol</full-title><abbr-1>The American journal of cardiology</abbr-1></periodical><alt-periodical><full-title>Am J Cardiol</full-title><abbr-1>The American journal of cardiology</abbr-1></alt-periodical><pages>450-8</pages><volume>57</volume><number>6</number><edition>1986/02/15</edition><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Autopsy</keyword><keyword>Cardiomegaly/*diagnosis/pathology</keyword><keyword>Echocardiography/*methods</keyword><keyword>Female</keyword><keyword>Heart Ventricles/pathology</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Organ Size</keyword></keywords><dates><year>1986</year><pub-dates><date>Feb 15</date></pub-dates></dates><isbn>0002-9149 (Print)&#xD;0002-9149 (Linking)</isbn><accession-num>2936235</accession-num><work-type>Comparative Study</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/2936235</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_25" \o "Devereux, 1986 #39" 25]  Right ventricle diastolic diameter and thickness of the free wall were measured in the apical view.  RV function in systole was evaluated from the tricuspid annular plane systolic excursion (TAPSE). ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_26" \o "Gladwin, 2004 #40" 26]
 Views of echocardiogram were taken at a epical view with the sample volume at the tip of the leaflet for pulsed Doppler of both the mitral and tricuspid valve. The early peak velocity (E wave) and the late atrial contraction wave (A wave), E/A ratio and deceleration time of E wave (DT) were measured. The calculation was made as the mean of three beats at end of inspiration and three at the end of expiration. The flow velocity of the upper pulmonary veins in the apical view was obtained in systolic and diastolic for forward flow velocity ratio (S/D).  The tissue Doppler of the lateral tricuspid annulus was obtained for systolic velocity (S), late diastolic velocity (A-) and the early filling velocity (E-). All data was taken in the apical four chamber view.
The intra-observer and inter-observer mean percentage error was calculated as absolute difference between measurements divided by the mean and expressed as the percentage of the pulsed Doppler measurements on echocardiogram. Pulmonary hypertension was defined as tricuspid valve velocity on continuous wave of e"2.5M/S  ADDIN EN.CITE <EndNote><Cite><Author>Berger</Author><Year>1985</Year><RecNum>93</RecNum><DisplayText>[27]</DisplayText><record><rec-number>93</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">93</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Berger, M.</author><author>Haimowitz, A.</author><author>Van Tosh, A.</author><author>Berdoff, R. L.</author><author>Goldberg, E.</author></authors></contributors><titles><title>Quantitative assessment of pulmonary hypertension in patients with tricuspid regurgitation using continuous wave Doppler ultrasound</title><secondary-title>J Am Coll Cardiol</secondary-title><alt-title>Journal of the American College of Cardiology</alt-title></titles><periodical><full-title>J Am Coll Cardiol</full-title><abbr-1>Journal of the American College of Cardiology</abbr-1></periodical><alt-periodical><full-title>J Am Coll Cardiol</full-title><abbr-1>Journal of the American College of Cardiology</abbr-1></alt-periodical><pages>359-65</pages><volume>6</volume><number>2</number><edition>1985/08/01</edition><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Blood Pressure</keyword><keyword>Cardiac Catheterization</keyword><keyword>*Echocardiography/methods</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Hypertension, Pulmonary/*diagnosis/physiopathology</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Pulmonary Artery/physiopathology</keyword><keyword>Systole</keyword><keyword>Tricuspid Valve Insufficiency/*diagnosis/physiopathology</keyword></keywords><dates><year>1985</year><pub-dates><date>Aug</date></pub-dates></dates><isbn>0735-1097 (Print)&#xD;0735-1097 (Linking)</isbn><accession-num>4019921</accession-num><work-type>Comparative Study</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/4019921</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_27" \o "Berger, 1985 #93" 27]. 


Statistical analysis
All data were entered and analysed using the Statistical Package of Social Sciences (SPSS) version 20. Data is presented as mean � SD.  Student t-test was used to analyse the differences between the mean variables of M mode for septal wall thickness of LV and RV cavity and wall thickness and LV mass index in the two groups and Chi-square analysis for frequency non-continuous data. 
Pearson correlation coefficient analysis was used to assess the linear association between concentrations of serum ferritin, pro BNP level and tricuspid valve velocity on CW Doppler.  Multiple regression analysis was applied to assess the odds ratio and predictive risk of different variables for the development of pulmonary hypertension in SCD patients. The variables  were; the  LV mass index of >121 gm/M2, Left atrial area >20 cm , E/E- ratio of > 13, S wave velocity of tissue Doppler <4 m/s, and DT of E wave <160 msec. on pulsed Doppler and serum ferritin >600 ng/l and Pro BNP >150 pmol/L.  All reported p-values were two tailed and p-value was regarded as significant at level of <0.05.
Results
 A one hundred and three patients with sickle cell disease were enrolled, the mean age of 28 � years (range 14-42) and sixty eight male (66.0 %). Table 1 shows the clinical characteristics of patients with SCD and the control group.  Patients with SCD compared with the control group had no difference in the age, gender, heart rate and systolic blood pressure.  Furthermore, haemoglobin level and serum ferritin and pro BNP were significantly different with high level of ferritin, pro BNP and low haemoglobin and diastolic blood pressure. 
Table 2 displays the echocardiographic measurements of M mode and 2 D of right and left ventricle.  Patients with SCD compared with the control, had significant increase in the right ventricle diameter and wall thickness as well as left atrium and left ventricle mass index. There was no significant differences noticed between the two groups for the left ventricle ejection fraction percentage and LV dimensions in systole and diastole. Tricuspid annular systolic excursion (TAPSE) was significantly higher confirming right ventricle systolic dysfunction.
Table 3 illustrates the both pulsed Doppler and tissue Doppler measurements for diastolic filling velocity in right and left ventricles as well as the tissue Doppler velocity of the tricuspid lateral annulus and ratio of velocity of pulmonary vein for systole and diastole. SCD patients had a significantly the  higher  pulsed Doppler  LV, higher  E/A  ratio, lower  A wave velocity  and  shorter  deceleration time of E wave (DT). Similarly the right ventricle showed A wave velocity significantly lower and DT shorter with higher E/A ratio.
Tissue Doppler of the lateral annulus of tricuspid valve  showed significantly shorter S wave velocity of   6.7�1.7 vs.11.3�1.9, p < 0.01, higher E/E- ratio of 12.2�1.2 vs.7.2�1.3, p< 0.05 and lower A- wave 5.3�1.6 vs.7.2�1.3, P=0.04.  The Ratio of right upper pulmonary vein systolic /diastolic velocity was significantly lower of 1.5 �0.12vs.2.4 � 0.11, p<0.01. On continuous wave Doppler velocity of  tricuspid valve showed significantly higher in the sickle cell disease patients of  2.9�0.14 vs.1.7�0.09, p<0.01 indicating higher pulmonary artery pressure with calculated right ventricle systolic pressure of  38.64 vs. 16.56 mmHg.
  In SCD patients there were 29/103 (28 %) patients with TVR of >2.5 m/s on continuous wave velocity, four (4%) of them had TVR >3 m/s and 70 (68%) patients had TVR <2.5 m/s.   There was a positive correlation between the serum level of ferritin, pro-BNP and tricuspid valve velocity of (r= 0.38) and (r=0.43) respectively. Figure 1 shows the percentage of patients in both groups based on TVR on continuous wave. 
Table 4 shows the odds ratio of pulmonary hypertension in SCD patients as follow, 3.1 for E/E- ratio >13, 2.5 for DT of <160 msec, 2.2 for LVMI >121 gm/M2, 1.9 for ferritin >600 ug/L, 1.3 for BNP >150 pmol/L, 1.7 for left atrial area >20cm and 1.4 for right ventricle wall thickness>3 mm.
Discussion
Chronic haemolytic anaemia is accompanied by a state of hyperkinetic circulation with tachycardia,  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_28" \o "Metivier, 2000 #42" 28] and the peripheral resistance is reduced with an increase of volume chambers and hypertrophy  ADDIN EN.CITE <EndNote><Cite><Author>Aessopos</Author><Year>2004</Year><RecNum>45</RecNum><DisplayText>[29]</DisplayText><record><rec-number>45</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">45</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Aessopos, A.</author><author>Deftereos, S.</author><author>Farmakis, D.</author><author>Corovesis, C.</author><author>Tassiopoulos, S.</author><author>Tsironi, M.</author><author>Georgonikou, D.</author><author>Moyssakis, J.</author></authors></contributors><auth-address>First Department of Internal Medicine, University of Athens Medical School, Athens, Greece. aaisopos@cc.uoa.gr</auth-address><titles><title>Cardiovascular adaptation to chronic anemia in the elderly: an echocardiographic study</title><secondary-title>Clin Invest Med</secondary-title><alt-title>Clinical and investigative medicine. Medecine clinique et experimentale</alt-title></titles><periodical><full-title>Clin Invest Med</full-title><abbr-1>Clinical and investigative medicine. Medecine clinique et experimentale</abbr-1></periodical><alt-periodical><full-title>Clin Invest Med</full-title><abbr-1>Clinical and investigative medicine. Medecine clinique et experimentale</abbr-1></alt-periodical><pages>265-73</pages><volume>27</volume><number>5</number><edition>2004/11/24</edition><keywords><keyword>*Adaptation, Physiological</keyword><keyword>Aged</keyword><keyword>Anemia/*physiopathology</keyword><keyword>*Cardiovascular Physiological Phenomena</keyword><keyword>Case-Control Studies</keyword><keyword>Chronic Disease</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Male</keyword></keywords><dates><year>2004</year><pub-dates><date>Oct</date></pub-dates></dates><isbn>0147-958X (Print)&#xD;0147-958X (Linking)</isbn><accession-num>15559863</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/15559863</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_29" \o "Aessopos, 2004 #45" 29].
In this study, patients with sickle cell disease had dilation of left atrium and right ventricle, greater left ventricle mass index and thicker RV wall compared with the control. The systolic function of left systolic ventricle had no difference between LVEF percent compared with control. However RV systolic function as assessed by TAPSE showed significant dysfunction than control. It is possible that these parameters of LVEF% are insensitive due to its load dependent relationship.   It has been observed that patients with SCD had higher preload and lower after load  ADDIN EN.CITE <EndNote><Cite><Author>Mandinov</Author><Year>1997</Year><RecNum>46</RecNum><DisplayText>[30]</DisplayText><record><rec-number>46</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">46</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Mandinov, L.</author><author>Kaufmann, P.</author><author>Brunner, F.</author><author>Hess, O. M.</author></authors></contributors><auth-address>Kardiologie, Inselspital, Bern.</auth-address><titles><title>[Anemia and heart function]</title><secondary-title>Praxis (Bern 1994)</secondary-title><alt-title>Praxis</alt-title></titles><periodical><full-title>Praxis (Bern 1994)</full-title><abbr-1>Praxis</abbr-1></periodical><alt-periodical><full-title>Praxis (Bern 1994)</full-title><abbr-1>Praxis</abbr-1></alt-periodical><pages>1687-92</pages><volume>86</volume><number>43</number><edition>1998/02/12</edition><keywords><keyword>Anemia/etiology/*physiopathology</keyword><keyword>Coronary Disease/physiopathology</keyword><keyword>Hemodynamics/*physiology</keyword><keyword>Hemoglobinometry</keyword><keyword>Humans</keyword><keyword>Hypertrophy, Left Ventricular/*physiopathology</keyword><keyword>Oxygen/blood</keyword><keyword>Ventricular Function, Left/physiology</keyword></keywords><dates><year>1997</year><pub-dates><date>Oct 22</date></pub-dates></dates><orig-pub>Anamie und Herzfunktion.</orig-pub><isbn>1661-8157 (Print)&#xD;1661-8157 (Linking)</isbn><accession-num>9432693</accession-num><work-type>Review</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/9432693</url></related-urls></urls><language>ger</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_30" \o "Mandinov, 1997 #46" 30] which cause higher diastolic filling and shorter DT of E which was observed  in our patients.  The RV dysfunction in this study may be due to lung involvement with predominant vaso-occlusive effect and the smaller RV mass than the left ventricle resulting in faster functional derangement. 
The diastolic filling pattern for both ventricles was suggestive of restrictive pattern with a significantly high E wave with shortened deceleration time. This is in keeping with one study by Appleton, et al.,  ADDIN EN.CITE <EndNote><Cite><Author>Appleton</Author><Year>1987</Year><RecNum>49</RecNum><DisplayText>[31]</DisplayText><record><rec-number>49</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">49</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Appleton, C. P.</author><author>Hatle, L. K.</author><author>Popp, R. L.</author></authors></contributors><auth-address>Cardiology Division, Stanford University School of Medicine, California 94305.</auth-address><titles><title>Superior vena cava and hepatic vein Doppler echocardiography in healthy adults</title><secondary-title>J Am Coll Cardiol</secondary-title><alt-title>Journal of the American College of Cardiology</alt-title></titles><periodical><full-title>J Am Coll Cardiol</full-title><abbr-1>Journal of the American College of Cardiology</abbr-1></periodical><alt-periodical><full-title>J Am Coll Cardiol</full-title><abbr-1>Journal of the American College of Cardiology</abbr-1></alt-periodical><pages>1032-9</pages><volume>10</volume><number>5</number><edition>1987/11/01</edition><keywords><keyword>Adult</keyword><keyword>Age Factors</keyword><keyword>Aged</keyword><keyword>Blood Flow Velocity</keyword><keyword>*Echocardiography</keyword><keyword>Heart Rate</keyword><keyword>Hepatic Veins/*physiology</keyword><keyword>Humans</keyword><keyword>Middle Aged</keyword><keyword>Myocardial Contraction</keyword><keyword>Respiration</keyword><keyword>Vena Cava, Superior/*physiology</keyword></keywords><dates><year>1987</year><pub-dates><date>Nov</date></pub-dates></dates><isbn>0735-1097 (Print)&#xD;0735-1097 (Linking)</isbn><accession-num>3668102</accession-num><work-type>Research Support, Non-U.S. Gov&apos;t&#xD;Research Support, U.S. Gov&apos;t, P.H.S.</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/3668102</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_31" \o "Appleton, 1987 #49" 31] where preload increment is associated with increase of early filling and shortened deceleration time. In two separate studies the diastolic pattern was mainly of abnormal relaxation pattern,  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_32" \o "Braden, 1996 #52" 32,  HYPERLINK \l "_ENREF_33" \o "Moyssakis, 2005 #22" 33] but the study population in both was a combined SCD and thalassemia.
The tissue Doppler of the tricuspid lateral annulus showed increase of E/E-ratio suggestive of higher RV end diastolic pressure with the reduction of S wave and A wave velocity. The tissue Doppler findings differs from one study that showed patients with SCD had higher tissue Doppler of A- but with higher E/E- ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_34" \o "Akgul, 2006 #55" 34].
The pulmonary vein systolic /diastolic velocity (S/D) ratio was significantly lower in patients with SCD. This is different from Moyssakis, et al.,  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_33" \o "Moyssakis, 2005 #22" 33] where S/D ratio was higher along with prolonged DT but with higher E/A ratio.  This difference in results may be due to the fact that patients population differences.  Patients with SCD had a lower acceleration time of <80 m sec   in pulmonary valve suggesting mild degree of pulmonary hypertension  ADDIN EN.CITE <EndNote><Cite><Author>Abdul-Mohsen</Author><Year>2012</Year><RecNum>60</RecNum><DisplayText>[35]</DisplayText><record><rec-number>60</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">60</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Abdul-Mohsen, M. F.</author></authors></contributors><auth-address>University of Dammam and King Fahd Hospital of the University, Dammam, PO Box 40032, Alkhobar 31952.</auth-address><titles><title>Echocardiographic evaluation of left ventricular diastolic and systolic function in Saudi patients with sickle cell disease</title><secondary-title>J Saudi Heart Assoc</secondary-title><alt-title>Journal of the Saudi Heart Association</alt-title></titles><periodical><full-title>J Saudi Heart Assoc</full-title><abbr-1>Journal of the Saudi Heart Association</abbr-1></periodical><alt-periodical><full-title>J Saudi Heart Assoc</full-title><abbr-1>Journal of the Saudi Heart Association</abbr-1></alt-periodical><pages>217-24</pages><volume>24</volume><number>4</number><edition>2013/11/01</edition><dates><year>2012</year><pub-dates><date>Oct</date></pub-dates></dates><isbn>1016-7315 (Print)&#xD;1016-7315 (Linking)</isbn><accession-num>24174829</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/24174829</url></related-urls></urls><custom2>3809466</custom2><electronic-resource-num>10.1016/j.jsha.2012.05.001</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_35" \o "Abdul-Mohsen, 2012 #60" 35]. There were 15/70 (22%) patients in the SCD group with pulmonary hypertension with TR velocity of e" 2. 5 m/s. The incidence of pulmonary hypertension of 22% in this study was lower than others where the incidences range between 33%-45 %  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_18" \o "Ataga, 2004 #28" 18].
The diastolic function may play a role in the development of pulmonary hypertension. In one study Sachdev et al., ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_36" \o "Sachdev, 2007 #76" 36] observed that diastolic dysfunction and PH can develop independently in patients with sickle cell anaemia where each contributing to increase mortality alone and patients with both risk factors have a poor prognosis.
The pathogenesis of PH in patients with SCD is multifactorial and may be due to sickling phenomena, vaso occlusive crises or acute chest syndrome. The repetitive intravascular haemolysis results in the release of haemoglobin that scavenges nitric oxide which finally lead to acute and chronic pulmonary vasoconstrictor  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_37" \o "Gladwin, 2003 #77" 37,  HYPERLINK \l "_ENREF_38" \o "Voskaridou, 2007 #75" 38].
The positive correlation between the ferritin, pro -BNP and TR velocity in this study support the notion that iron overload  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_39" \o "Lin, 2001 #78" 39] and dilation of the ventricular chambers are implicated in the pathogenesis of pulmonary hypertension  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_40" \o "Aessopos, 2005 #89" 40].  Multiple regression analysis indicated that the most sensitive marker for the development of pulmonary hypertension in SCD is the E/E- ratio>13 with odds ratio of 3.1 followed by DT <2.5, LVMI >121gm/M2 of 2.2, ferritin >600 (g/L of 1.9, left atrial area >20 cm of 1.7 and pro-BNP > 150 pmol/L of 1.3.
In one study on SCD patients and beta thalassemia, pulmonary artery pressure was positively correlated with left atrial area, diastolic dysfunction and high serum level of NT pro BNP  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_41" \o "Machado, 2006 #87" 41]. In another study by Oguanobi NI et al.,  ADDIN EN.CITE <EndNote><Cite><Author>Oguanobi</Author><Year>2012</Year><RecNum>2</RecNum><DisplayText>[42]</DisplayText><record><rec-number>2</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">2</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Oguanobi, N. I.</author><author>Ejim, E. C.</author><author>Anisiuba, B. C.</author><author>Onwubere, B. J.</author><author>Ike, S. O.</author><author>Ibegbulam, O. G.</author><author>Agwu, O.</author></authors></contributors><auth-address>Department of Medicine, University of Nigeria Teaching Hospital, Enugu, Nigeria.</auth-address><titles><title>Clinical and electrocardiographic evaluation of sickle-cell anaemia patients with pulmonary hypertension</title><secondary-title>ISRN Hematol</secondary-title><alt-title>ISRN hematology</alt-title></titles><periodical><full-title>ISRN Hematol</full-title><abbr-1>ISRN hematology</abbr-1></periodical><alt-periodical><full-title>ISRN Hematol</full-title><abbr-1>ISRN hematology</abbr-1></alt-periodical><pages>768718</pages><volume>2012</volume><edition>2012/04/27</edition><dates><year>2012</year></dates><isbn>2090-4428 (Electronic)&#xD;2090-441X (Linking)</isbn><accession-num>22536523</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/22536523</url></related-urls></urls><custom2>3320006</custom2><electronic-resource-num>10.5402/2012/768718</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_42" \o "Oguanobi, 2012 #2" 42] patients with SCD were evaluated clinically with echocardiogram for development of pulmonary hypertension. The ECG variables were significantly associated with PH such as right ventricle hypertrophy, increased P wave duration and increased QTC dispersion time.  
Conclusion
Adult patients with SCD have RV dilation and increase wall thickness. The LV systolic function is normal but with diastolic dysfunction suggestive of restrictive pattern. Thirty three percent of patients had significant pulmonary hypertension. There was a positive correlation between ferritin, pro BNP level and the risk of pulmonary hypertension. The risk of PAH development in SCD patients is higher if the shorter DT <160 msec, LVMI >121 gm/M2, left atrial area >20 cm, E/E- ratio e" 13 and RV wall thickness >3 mm.

Acknowledgment
This study has been supported by a grant from the Arabian Gulf University, Kingdom of Bahrain.
Table 1.   Clinical characteristics of the study population, data presented as the mean �SD.
Characteristics SCD
N=103Control 
N=103P value Age 28.52�9.1129.74�8.710.64Male  68(66%)66(64.0%)0.76Heart rate /min 72.65�8.2371.42�8.330.97SBP  mmHg 128.47�7.92124.58�8.650.85DBP  mmHg67.84�4.5575.25�3.880.042Haemoglobin (g/dl)9.3�1.213.2�1.50.01Serum ferritin  ug/L 423.25�98.2386.12�16.340.01Serum pro BNP pmol/L 365.76�96.3498.54�19.580.01
Abbreviations: SBP, systolic blood pressure, DBP diastolic blood pressure, SCD, sickle cell disease. 

Table 2. The M mode and 2 �D echocardiographic data in the study population, the data was presented as mean value �SD.
 SCD
N=103Control 
N=103P value LA   area (cm)22.21�4.2216.72� 3.900.042LVEDD(cm)5.51� 0.324.72�0.350.361LVESD(cm)3.63�0.243.12�0.310.653LV mass index  gm/M2105�10.383�7.10.001RV diameter(cm)2.8�0.422.4�0.310.043RV wall thickness (mm)0.34�0.060.28�0.030.024LVEF percentage 58.90�4.761.22�3.90.061RV TAPSE(mm)1.42�0.211.11�0.230.023
Abbreviations: LA: left Atrium, LVEDD: left ventricle end diastolic dimension, LVESD: left ventricle end systolic dimension, EF%: ejection fraction Percentage, TAPES: tricuspid annulus plane excursions. 
Table 3. Pulsed and tissue Doppler parameters in the study population, data presented as mean �SD.
Parameters Patients with SCD
N=103Control  patients
N=103P value LV E wave (mcec)85.23�1.9262.43�1.670.001LV A wave (msec)46.26�4.756.24�3.20.032LV E/A1.86�0.011.10 �0.030.024LVDT of E wave  (msec)156.43�23.5189.87�19.50.031RV E wave (cm/s076.65�1.4359.34�1.90.04RV A wave (cm/s)40.65�3.549.65�3.40.043RV E/A1.93 �0.031.20�0.020.076RV DT of E wave (msec)176.24�21.4210.43�0.240.012RV pulmonic vein S/D ratio.1.5 �0.122.4�0.110.002PV acc T (msec)94.24�11.3110.14�14.80.041Tricuspid CW velocity (m/s)2.9�0.141.7�0.090.004Tissue Doppler S wave 6.7�1.711.3�1.90.01TD of  E/E - ratio12.2�1.27.2�1.30.04TD of A � wave 5.3�1.67.2�1.20.02
Abbreviations: SCD: sickle cell disease, LV: left ventricle, RV: right ventricle, E: pulsed Doppler early diastolic filling, A atrial diastolic filling, DT: deceleration time of E wave, E- (tissue Doppler E wave), A- (tissue Doppler of A wave, S/D: systolic /diastolic wave ratio, S: systolic wave. accT (acceleration time of pulmonary valve.

Table 4. Odds ratio of multiple regression analysis of different pulsed and tissue Doppler variables in the prediction of pulmonary hypertension in patients with Sickle cell disease with TVR >2.5 M/S. 
Odds ratio P value Pro-BNP> 150 pmol /L 1.3(0.7-1.9)P=0.01Ferritin  600  ng /ml1.9(1.1-2.7)P=0.03E/E- >133.1(2.5-3.7)P=0.01DT<160  msec2.5(2.0-3.0)P=0.01LV M I>121 gm /M22.2(1.6-2.8)P=0.01Left atrial area  >20 cm 1.7(1.2-2.2)P=0.01Right ventricle wall >3 mm 1.4(1.0-1.8)0=0.04
Abbreviations: (DT) deceleration time , (LVMI) left ventricle mass index,( E/E- ) early filling wave of pulsed Doppler to tissue Doppler E wave, (BNP )brain natriuretic peptide. (TVR) tricuspid vale regurgitation. (PAH) pulmonary hypertension.


Figure 1 .  The percentage of patients included in each based on results of variables of pulse and tissue Doppler echo, group 1(n=34) with tricuspid valve velocity of e"2.5 m/s and group 2(n=70) TVR<2.5 m/s

Abbreviations: DT: deceleration Time, LVMI: left ventricle mass index, E/E- : Early filling wave on Pulsed Doppler / Tissue Doppler, BNP: brain Natriuretic peptide. 


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36.	V. Sachdev, R. F. Machado, Y. Shizukuda, Y. N. Rao, S. Sidenko, I. Ernst et al. Diastolic dysfunction is an independent risk factor for death in patients with sickle ce167lpxy|���־��v�^F�.�F.hZ)hE�5�CJOJQJ\�^JaJmH	sH	.hZ)hdI5�CJOJQJ\�^JaJmH	sH	.hZ)h�5�CJOJQJ\�^JaJmH	sH	.hZ)h�|d5�CJOJQJ\�^JaJmH	sH	.hZ)hz95�CJOJQJ\�^JaJmH	sH	.hZ)hN�5�CJOJQJ\�^JaJmH	sH	.hZ)h\V5�CJOJQJ\�^JaJmH	sH	(hm]\h�CJOJQJ^JaJmH	sH	(h3Jh�CJOJQJ^JaJmH	sH	
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6�OJQJ^JaJmHnHull disease. J Am Coll Cardiol. 2007; 49(4): 472-9. 10.1016/j.jacc.2006.09.038   HYPERLINK "http://www.ncbi.nlm.nih.gov/pubmed/17258093" http://www.ncbi.nlm.nih.gov/pubmed/17258093
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{J?޴y��_(�LFy^{���l�'cO��U�E����v�=u;m��B�G.^��[��8�9,� ���kG�հ'aI��#���S��g��Z��/+�=�o^�=���OmOI���T~��1z;��mm#{j���&�b��XN��U�F����jĮ��9j�+�kaa����b(W�x/l.��8�܌U��ϩ��'�J@��H�Ӷb�(��q��1�<�2�N%Q��.�M�\���kӖ�80��jll��v3�_��]s
�?���>a0������2}���ր�T�Â�^�:|jNm�9؆W��~x.��1�엫����C�ɗ����7!}���a��?��A�C�����|�b{�W���@T�� ���)sD���y������K�	_ENREF_1�D<EndNote><Cite><Author>Platt</Author><Year>1994</Year><RecNum>6</RecNum><DisplayText>[2]</DisplayText><record><rec-number>6</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">6</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Platt, O. S.</author><author>Brambilla, D. J.</author><author>Rosse, W. F.</author><author>Milner, P. F.</author><author>Castro, O.</author><author>Steinberg, M. H.</author><author>Klug, P. P.</author></authors></contributors><auth-address>Department of Medicine, Children&apos;s Hospital, Boston, MA 02115.</auth-address><titles><title>Mortality in sickle cell disease. Life expectancy and risk factors for early death</title><secondary-title>N Engl J Med</secondary-title><alt-title>The New England journal of medicine</alt-title></titles><periodical><full-title>N Engl J Med</full-title><abbr-1>The New England journal of medicine</abbr-1></periodical><alt-periodical><full-title>N Engl J Med</full-title><abbr-1>The New England journal of medicine</abbr-1></alt-periodical><pages>1639-44</pages><volume>330</volume><number>23</number><edition>1994/06/09</edition><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Anemia, Sickle Cell/*mortality</keyword><keyword>Cause of Death</keyword><keyword>Child</keyword><keyword>Female</keyword><keyword>Hemoglobin SC Disease/*mortality</keyword><keyword>Humans</keyword><keyword>*Life Expectancy</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Probability</keyword><keyword>Regression Analysis</keyword><keyword>Risk Factors</keyword><keyword>Survival Analysis</keyword><keyword>beta-Thalassemia/mortality</keyword></keywords><dates><year>1994</year><pub-dates><date>Jun 9</date></pub-dates></dates><isbn>0028-4793 (Print)&#xD;0028-4793 (Linking)</isbn><accession-num>7993409</accession-num><work-type>Research Support, U.S. Gov&apos;t, P.H.S.</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/7993409</url></related-urls></urls><electronic-resource-num>10.1056/NEJM199406093302303</electronic-resource-num><language>eng</language></record></Cite></EndNote>�D<EndNote><Cite><Author>Platt</Author><Year>1994</Year><RecNum>6</RecNum><DisplayText>[2]</DisplayText><record><rec-number>6</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">6</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Platt, O. S.</author><author>Brambilla, D. J.</author><author>Rosse, W. F.</author><author>Milner, P. F.</author><author>Castro, O.</author><author>Steinberg, M. H.</author><author>Klug, P. P.</author></authors></contributors><auth-address>Department of Medicine, Children&apos;s Hospital, Boston, MA 02115.</auth-address><titles><title>Mortality in sickle cell disease. Life expectancy and risk factors for early death</title><secondary-title>N Engl J Med</secondary-title><alt-title>The New England journal of medicine</alt-title></titles><periodical><full-title>N Engl J Med</full-title><abbr-1>The New England journal of medicine</abbr-1></periodical><alt-periodical><full-title>N Engl J Med</full-title><abbr-1>The New England journal of medicine</abbr-1></alt-periodical><pages>1639-44</pages><volume>330</volume><number>23</number><edition>1994/06/09</edition><keywords><keyword>Adult</keyword><keyword>Aged</keyword><keyword>Anemia, Sickle Cell/*mortality</keyword><keyword>Cause of Death</keyword><keyword>Child</keyword><keyword>Female</keyword><keyword>Hemoglobin SC Disease/*mortality</keyword><keyword>Humans</keyword><keyword>*Life Expectancy</keyword><keyword>Male</keyword><keyword>Middle Aged</keyword><keyword>Probability</keyword><keyword>Regression Analysis</keyword><keyword>Risk Factors</keyword><keyword>Survival Analysis</keyword><keyword>beta-Thalassemia/mortality</keyword></keywords><dates><year>1994</year><pub-dates><date>Jun 9</date></pub-dates></dates><isbn>0028-4793 (Print)&#xD;0028-4793 (Linking)</isbn><accession-num>7993409</accession-num><work-type>Research Support, U.S. Gov&apos;t, P.H.S.</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/7993409</url></related-urls></urls><electronic-resource-num>10.1056/NEJM199406093302303</electronic-resource-num><language>eng</language></record></Cite></EndNote>sD���y������K�	_ENREF_2�
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J.</author></authors></contributors><auth-address>Non-Communicable Disease Program, Ministry of Health, Kingdom of Saudi Arabia.</auth-address><titles><title>Premarital screening for thalassemia and sickle cell disease in Saudi Arabia</title><secondary-title>Genet Med</secondary-title><alt-title>Genetics in medicine : official journal of the American College of Medical Genetics</alt-title></titles><periodical><full-title>Genet Med</full-title><abbr-1>Genetics in medicine : official journal of the American College of Medical Genetics</abbr-1></periodical><alt-periodical><full-title>Genet Med</full-title><abbr-1>Genetics in medicine : official journal of the American College of Medical Genetics</abbr-1></alt-periodical><pages>372-7</pages><volume>9</volume><number>6</number><edition>2007/06/19</edition><keywords><keyword>Anemia, Sickle Cell/epidemiology/*genetics</keyword><keyword>Female</keyword><keyword>*Genetic Testing</keyword><keyword>Humans</keyword><keyword>Male</keyword><keyword>*Premarital Examinations</keyword><keyword>Saudi Arabia</keyword><keyword>Thalassemia/epidemiology/*genetics</keyword></keywords><dates><year>2007</year><pub-dates><date>Jun</date></pub-dates></dates><isbn>1098-3600 (Print)&#xD;1098-3600 (Linking)</isbn><accession-num>17575503</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/17575503</url></related-urls></urls><electronic-resource-num>10.1097GIM.0b013e318065a9e8</electronic-resource-num><language>eng</language></record></Cite><Cite><Author>Nasserullah</Author><Year>2003</Year><RecNum>9</RecNum><record><rec-number>9</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">9</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Nasserullah, Z.</author><author>Alshammari, A.</author><author>Abbas, M. 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A.</author></authors></contributors><auth-address>Qatif Central Hospital, Qatif, Saudi Arabia and Dammam Maternity and Children Hospital, Dammam, Saudi Arabia.</auth-address><titles><title>Regional experience with newborn screening for sickle cell disease, other hemoglobinopathies and G6PD deficiency</title><secondary-title>Ann Saudi Med</secondary-title><alt-title>Annals of Saudi medicine</alt-title></titles><periodical><full-title>Ann Saudi Med</full-title><abbr-1>Annals of Saudi medicine</abbr-1></periodical><alt-periodical><full-title>Ann Saudi Med</full-title><abbr-1>Annals of Saudi medicine</abbr-1></alt-periodical><pages>354-7</pages><volume>23</volume><number>6</number><edition>2006/07/27</edition><dates><year>2003</year><pub-dates><date>Nov-Dec</date></pub-dates></dates><isbn>0256-4947 (Print)&#xD;0256-4947 (Linking)</isbn><accession-num>16868367</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/16868367</url></related-urls></urls><language>eng</language></record></Cite></EndNote>sD���y������K�	_ENREF_3sD���y������K�	_ENREF_4�D<EndNote><Cite><Author>el-Hazmi</Author><Year>1996</Year><RecNum>10</RecNum><DisplayText>[5, 6]</DisplayText><record><rec-number>10</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">10</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>el-Hazmi, M. 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C.</author></authors></contributors><auth-address>Division of Cardiology, Children&apos;s Hospital of Los Angeles and LAC+USC Medical Center, Los Angeles, California, USA. abatra@iupui.edu</auth-address><titles><title>Cardiac abnormalities in children with sickle cell anemia</title><secondary-title>Am J Hematol</secondary-title><alt-title>American journal of hematology</alt-title></titles><periodical><full-title>Am J Hematol</full-title><abbr-1>American journal of hematology</abbr-1></periodical><alt-periodical><full-title>Am J Hematol</full-title><abbr-1>American journal of hematology</abbr-1></alt-periodical><pages>306-12</pages><volume>70</volume><number>4</number><edition>2002/09/05</edition><keywords><keyword>Adolescent</keyword><keyword>Adult</keyword><keyword>Anemia, Sickle Cell/*complications/pathology</keyword><keyword>Child</keyword><keyword>Child, Preschool</keyword><keyword>Female</keyword><keyword>Ferritins/blood</keyword><keyword>Heart Defects, Congenital/*diagnosis/*etiology</keyword><keyword>Heart Function Tests</keyword><keyword>Humans</keyword><keyword>Iron Overload</keyword><keyword>Male</keyword><keyword>Prospective Studies</keyword><keyword>Severity of Illness Index</keyword></keywords><dates><year>2002</year><pub-dates><date>Aug</date></pub-dates></dates><isbn>0361-8609 (Print)&#xD;0361-8609 (Linking)</isbn><accession-num>12210812</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/12210812</url></related-urls></urls><electronic-resource-num>10.1002/ajh.10154</electronic-resource-num><language>eng</language></record></Cite><Cite><Author>Zilberman</Author><Year>2007</Year><RecNum>12</RecNum><record><rec-number>12</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">12</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Zilberman, M. 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C.</author></authors></contributors><auth-address>Division of Cardiology, Children&apos;s Hospital of Los Angeles and LAC+USC Medical Center, Los Angeles, California, USA. abatra@iupui.edu</auth-address><titles><title>Cardiac abnormalities in children with sickle cell anemia</title><secondary-title>Am J Hematol</secondary-title><alt-title>American journal of hematology</alt-title></titles><periodical><full-title>Am J Hematol</full-title><abbr-1>American journal of hematology</abbr-1></periodical><alt-periodical><full-title>Am J Hematol</full-title><abbr-1>American journal of hematology</abbr-1></alt-periodical><pages>306-12</pages><volume>70</volume><number>4</number><edition>2002/09/05</edition><keywords><keyword>Adolescent</keyword><keyword>Adult</keyword><keyword>Anemia, Sickle Cell/*complications/pathology</keyword><keyword>Child</keyword><keyword>Child, Preschool</keyword><keyword>Female</keyword><keyword>Ferritins/blood</keyword><keyword>Heart Defects, Congenital/*diagnosis/*etiology</keyword><keyword>Heart Function Tests</keyword><keyword>Humans</keyword><keyword>Iron Overload</keyword><keyword>Male</keyword><keyword>Prospective Studies</keyword><keyword>Severity of Illness Index</keyword></keywords><dates><year>2002</year><pub-dates><date>Aug</date></pub-dates></dates><isbn>0361-8609 (Print)&#xD;0361-8609 (Linking)</isbn><accession-num>12210812</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/12210812</url></related-urls></urls><electronic-resource-num>10.1002/ajh.10154</electronic-resource-num><language>eng</language></record></Cite><Cite><Author>Zilberman</Author><Year>2007</Year><RecNum>12</RecNum><record><rec-number>12</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">12</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Zilberman, M. 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A.</author></authors></contributors><auth-address>Department of Pediatrics, Wayne State University School of Medicine, Detroit, Michigan, USA. mzilberm@dmc.org</auth-address><titles><title>Evaluation of left ventricular diastolic function in pediatric sickle cell disease patients</title><secondary-title>Am J Hematol</secondary-title><alt-title>American journal of hematology</alt-title></titles><periodical><full-title>Am J Hematol</full-title><abbr-1>American journal of hematology</abbr-1></periodical><alt-periodical><full-title>Am J Hematol</full-title><abbr-1>American journal of hematology</abbr-1></alt-periodical><pages>433-8</pages><volume>82</volume><number>6</number><edition>2007/02/03</edition><keywords><keyword>Adolescent</keyword><keyword>Age Factors</keyword><keyword>Anemia, Sickle Cell/complications/*physiopathology</keyword><keyword>Child</keyword><keyword>Echocardiography, Doppler</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Hypertrophy, Left Ventricular/complications/*physiopathology/ultrasonography</keyword><keyword>Male</keyword><keyword>Predictive Value of Tests</keyword><keyword>Sensitivity and Specificity</keyword><keyword>Ventricular Dysfunction, Left/complications/*physiopathology/ultrasonography</keyword></keywords><dates><year>2007</year><pub-dates><date>Jun</date></pub-dates></dates><isbn>0361-8609 (Print)&#xD;0361-8609 (Linking)</isbn><accession-num>17266053</accession-num><work-type>Research Support, Non-U.S. Gov&apos;t</work-type><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/17266053</url></related-urls></urls><electronic-resource-num>10.1002/ajh.20866</electronic-resource-num><language>eng</language></record></Cite></EndNote>sD���y������K�	_ENREF_7sD���y������K�	_ENREF_8@D<EndNote><Cite><Author>Bahl</Author><Year>1992</Year><RecNum>14</RecNum><DisplayText>[9, 10]</DisplayText><record><rec-number>14</rec-number><foreign-keys><key app="EN" db-id="f2zwfv9djxp2atevpac5ddswa0x555te992a">14</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Bahl, V. 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