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IOSR Journal of Dental and Medical Sciences (IOSR-JDMS)
e-ISSN: 2279-0853, p-ISSN: 2279-0861.Volume 14, Issue 11 Ver. V (Nov. 2015), PP 11-16
www.iosrjournals.org
DOI: 10.9790/0853-141151116 www.iosrjournals.org 11 | Page
Ocular Manifestations In Sickle Cell Disease – A Preventable
Cause Of Blindness?
Kaushika Rautray1
, Pravin Tidake2
, Sourya Acharya3
, Samarth Shukla4
1, Primary researcher , MBBS 2,Professor, Dept. Of Opthalmology 3, Professor, Dept. of Medicine
4,Professor, Dept . of Pathology
JN Medical College, DMIMS University Sawangi ( Meghe) Wardha-442004 Maharashtra
Address for Correspondence; Dr. Sourya Acharya
Abstract:
Aim: To study the co-relation between hematologic parameters and ophthalmic manifestations in patients of
sickle cell disease (SCD).
Methods : This study was conducted in Acharya Vinoba Bhave Rural Hospital, JN medical College, Wardha.
All the patients coming regularly to sickle cell O.P.D for follow up and those who were admitted for sickle cell
crisis in medicine ward , obstetrics/gynecology patients who were found to be sickle cell positive (SS pattern)
and pediatric patients diagnosed with sickle cell disease were included for this study. A total of 35 sickle cell
disease (SCD) patients were studied. Hematologic investigations were done and ophthalmic investigations such
as visual acuity, silt lamp bio-microscopy and fundoscopy was done and compared. For statistical analysis
SPSS software was used.
Results: The study showed that 70% of the Sickle cell disease patients with hemoglobin 6 gm % or less had
some ocular abnormality.
Conclusion : All sickle cell disease patients should have regular ophthalmic examination to prevent the risk of
sickle cell retinopathy.
Key words : Sickle cell disease , SS pattern, sickle cell retinopathy
I. Introduction
In India, haemoglobinopathies have been considered responsible for the largest number of genetic
disorders and hence contribute to the imbalance in the health profile of the nation.
The cumulative gene frequency of haemoglobinopathies in India is 4.2%. With a population of over 1
billion and a birth rate of 28 per 1000, there are over 42 million carriers and over 12,000 infants are born each
year with a major and clinical significant haemoglobinopathy. (4, 5, 6)
Despite being characterized by the same point mutation, the clinical course of Sickle Cell Disease
(SCD) is extremely variable, ranging from mild to very severe depending on the different genotypes. (7, 8, 9, 10)
Painful crisis and severe hemolytic anemia are the two most common systemic complications.
However, ocular manifestations are usually mild and asymptomatic. Ocular changes such as conjunctival
sickling sign at the conjunctiva (11, 12, 13, 14)
and iris atrophy have been noticed. Changes over the other vascular
regions of the eye are seen in the choroid, optic disc, and the retina (15)
.Though nearly all structures in the eye
are affected in Sickle cell disease but, the vision threatening problems are due to retinal neovascularization.(17,18)
Sickle cell retinopathy develops in up to 42% of individuals during the second decade of life. (16)
A complication of proliferative sickle cell retinopathy (PSCR) is a major contributor for vision loss and
visual impairment in 10-20% of affected eyes. (19, 20, 21)
Micro-vascular occlusions being the most common cause of visual loss, it is logical then to assume that
Sickle cell disease patients who suffer repeated episodes of vasocclusion are vulnerable to visual loss causing
blindness. The number of patients who suffer vasocculsive crisis is unclear. The purpose of this study is to
document early ocular abnormalities in sickle cell patients and to suggest the need for earlier ophthalmic
screening.
II. Aims And Objectives
To study the ocular pathologies in sickle cell disease and correlate them with hematological parameters.
Ocular manifestations in sickle cell disease – A preventable cause of blindness?
DOI: 10.9790/0853-141151116 www.iosrjournals.org 12 | Page
III. Methodology
Site Setting – This was a cross sectional study conducted in Acharya Vinobha Bhave Rural Hospital
(A.V.B.R.H), a 909 bedded rural tertiary hospital of Datta Meghe Institute Of Medical Sciences(DMIMS)
sawangi(Meghe), Wardha. The study was conducted over a period of 2 months, with due clearance of
institutional ethical committee.
1. Study Population – All diagnosed cases of sickle cell disease (by Hb electrophoresis) in AVBRH were
examined for ocular manifestations.
Sample Size – 36
Inclusion Criteria –
 Sickle cell patients who came for regular follow up/admitted for sickle cell crisis.
Exclusion Criteria –
 Anemias other than sickle cell disease.
 Patients with sickle cell trait, sickle cell thalassaemia and other genetic hemoglobinopathies other than sickle
cell disease.
Procedure/Proposed Intervention
 All patients confirmed sickle cell on Hb electrophoresis were included in this study.
 Complete blood counts , Hemoglobin, red cell indices, white cell count and platelet count were done.
 Detailed ocular examination as follows: assessment of visual acuity using Snellen‘s chart. Anterior segment
structure viz conjunctiva, cornea, iris and lens was examined using silt lamp examination.
 Indirect ophthalmoscopy were carried out for lesions in posterior segment.20 D lens was used to examine the
peripheral retina.
 Fundus examination with binocular indirect ophthalmoscope and silt lamp biomicroscopy.78 D and 90 D lens
was used in silt lamp biomicroscopy to examine optic disc changes and macular changes.
 Color photographs by fundus camera and fluorescien angiography (FFA) were done in cases with suspected
proliferative sickle retinopathy. Goldberg classification was followed for classifying sickle cell retinopathy if
present.
Statistical Analysis
SPSS software was used for statistically analyzing the collected data and results obtained will be interpreted in
the form of tables, graphs and charts.
IV. Observations And Results
Table 1: Comparison of parameters in positive and negative patients
Student‘s unpaired t test
N Mean Std. Deviation
Std. Error
Mean
t-value p-value
Hb%
Positive 7 4.00 0.42 0.16
5.38 0.0001,S,p<0.05
Negative 28 8.55 2.20 0.41
Total RBC
Positive 7 1.91 0.77 0.29
4.50 0.0001,S,p<0.05
Negative 28 3.44 0.81 0.15
RDW
Positive 7 26.40 2.01 0.76
10.63 0.0001,S,p<0.05
Negative 28 17.13 2.07 0.39
Total WBC
Positive 7 2857.14 468.53 177.08
3.79 0.001,S,p<0.05
Negative 28 7646.42 3297.64 623.19
MCV
Positive 7 91.28 4.85 1.83
5.27 0.0001,S,p<0.05
Negative 28 72.57 8.99 1.69
MCH
Positive 7 28.82 2.84 1.07
0.29 0.76,NS,p>0.05
Negative 28 28.34 4.05 0.76
MCHC
Positive 7 33.28 1.66 0.63
0.54 0.58,NS,p>0.05
Negative 28 32.791 2.22 0.42
Platelet Count
Positive 6 1.69 0.11 0.04
2.79 0.009,S,p<0.05
Negative 27 3.00 1.13 0.21
Ocular manifestations in sickle cell disease – A preventable cause of blindness?
DOI: 10.9790/0853-141151116 www.iosrjournals.org 13 | Page
Table 2: Correlation of Hb% with other clinical parameters
Pearson‘s Correlation Coefficient
Parameters Mean Std. Deviation N Correlation ‗r‘ p-value
Hb% 7.64 2.70 35 - -
Total RBC 3.14 1.00 35 0.64 0.001,S
RDW 18.99 4.27 35 -0.50 0.002,S
Total WBC 6688.57 3528.77 35 0.40 0.014,S
MCV 76.31 11.22 35 -0.53 0.001,S
MCH 28.44 3.81 35 -0.12 0.45,NS
MCHC 32.89 2.11 35 0.12 0.48,NS
Platelet Count 2.76 1.14 33 0.50 0.003,S
Ocular manifestations in sickle cell disease – A preventable cause of blindness?
DOI: 10.9790/0853-141151116 www.iosrjournals.org 14 | Page
Table 3: Ocular Incidence According To Hemoglobin Concentration
Hemoglobin Range Sickle Cell Disease
Total Cases No. with Ocular Changes %
Less than 6 gm% (Severe) 10 7 70
6 – 10 gm% (Moderate) 18 0 0
10 – 13 gm% (Mild) 8 0 0
Above 13 gm% 0 0 0
Table 4: Ocular Manifestations
Ocular Manifestations
Fundus in General
Sickle Cell Disease
No. of Cases with Ocular changes
n = 7
%
Major retinal vessel changes 2 28.57
Hemorrhages in periphery 4 57.14
Neovascularisation 1 14.28
Iridescent glistening vessels - 0
Peripheral vessel deposits - 0
Chorioditis - 0
V. Discussion
Sickle cell haemoglobinopathy is a common disorder of this area. Irrespective of any ocular
complaints, a search was made for ocular changes amongst the 36 sickle positive patients. Despite the fact that
none of them had any ocular symptoms, but various ocular signs were found in them. All the patients except one
who had been admitted for vision defect and was found to have neovascularisation.
Out of the 36 sickle positive patients, 26 cases (72.22%) were below 30 years of age, the youngest
patient being 7 years old. There was one case of sickle cell anemia after 40 years. Seventeen patients were male
and 19 were of the females (57.16%). Females were more affected than males. Goldberg et al and Condon et al
had also observed such sex predilection in their cases. The caste distribution was majority were from religion
buddha (61.11%), Teli (27.77%), goud (11.11%).
It should be noted that 70% of the Sickle cell patients were found with less that hemoglobin 6 gm %
had some ocular changes. Pallor, icterus and vascular changes (90.47%) were observed in the conjunctiva. The
vascular changes were of grade I and consisted of comma shaped or cork screw shaped or abnormally long,
linear dilatations of vessels still connected to the vascular network with sludged flow, mostly observed in the
bulbar conjunctiva covered by lids.
Kate et a1and Condon et al (97.4% in Hb-SS cases) have observed such changes in various degree in
sickle cell anemia and sickle cell Hb-C disease other than sickle cell trait. Significant changes were observed in
major retinal vessels (28.57%). The major retinal vessels were dilated, full and tortuous, the veins being more
tortuous than arteries. In some cases, the arteries were pale and narrow. The peripheral vessels were tortuous
and sometimes occluded, but in a few cases, the arterioles were chalky white in color, associated with
perivascular sheathing, occlusion and tortuosity.
Ocular manifestations in sickle cell disease – A preventable cause of blindness?
DOI: 10.9790/0853-141151116 www.iosrjournals.org 15 | Page
Similar findings have been documented by Condon et al, who found peripheral vessel disease 93.4%
and major retinal vessel changes in 10.5% of Hb. SS cases; whereas Kate et a1have found venous fullness and
venous tortuosity in 18% and 24% of their series. Hemorrhage (57.14%) and neovascularisation (14.28%) were
also observed in the peripheral retina. Condon et al; had noted retinal hemorrhage (2.6%) and tortuosity and
dilatations of capillary network with micro-aneurysmal formation and neovascularisation (39.5%) in the Hb-SS
cases of his study, but Kate et al did not get any case of retinal hemorrhage in their series (instead they had
observed vitreous hemorrhage in one case). Majority of cases with ocular involvement in all categories of
haemoglobinopathies were within the third decades of life although highest incidence occurred in the second
decade as observed in this study. Goldberg et al had observed the mean age for the ocular changes as 28 years,
while Condon et al had seen maximum changes in 10-20 years. His study in Jamaica in elderly age
groupsshowed that incidence of peripheral vessel disease appears to increase with age. Majority of cases of
different haemoglobinopathies had ocular changes in moderate and severe degree of anemia (less than 6 gm. %
of hemoglobin). But the comparison of the prevalence of ocular changes in different hemoglobin concentrations
and in various haemoglobinopathies, of this study, indicates that besides anemia, the abnormal sickle
hemoglobin is the prime cause for the ocular changes in this disorder (e.g. in 6-10 gm.% of hemoglobin range,
indicating that simple anemia is not the only cause).
VI. Conclusion
Sickle cell disease is a disease of national concern. Its complication continue to remain as a significant
issue to physicians.
Visual loss which occurs due to vasocculsive crises can be prevented in patients of sickle cell disease
by early ocular diagnosis as it would seem, logical to assume that patients with SCD who suffer from repeated
episodes of vaso-occlussion might be most vulnerable to ocular pathology.
Therefore, this study attempts to include ocular examination in routine investigation of sickle cell tests
and in routine follow up check-ups in diagnosed cases of sickle cell disease. Thus, protecting them from visual
impairment and visual loss.
References
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Ocular Manifestations In Sickle Cell Disease – A Preventable Cause Of Blindness?

  • 1. IOSR Journal of Dental and Medical Sciences (IOSR-JDMS) e-ISSN: 2279-0853, p-ISSN: 2279-0861.Volume 14, Issue 11 Ver. V (Nov. 2015), PP 11-16 www.iosrjournals.org DOI: 10.9790/0853-141151116 www.iosrjournals.org 11 | Page Ocular Manifestations In Sickle Cell Disease – A Preventable Cause Of Blindness? Kaushika Rautray1 , Pravin Tidake2 , Sourya Acharya3 , Samarth Shukla4 1, Primary researcher , MBBS 2,Professor, Dept. Of Opthalmology 3, Professor, Dept. of Medicine 4,Professor, Dept . of Pathology JN Medical College, DMIMS University Sawangi ( Meghe) Wardha-442004 Maharashtra Address for Correspondence; Dr. Sourya Acharya Abstract: Aim: To study the co-relation between hematologic parameters and ophthalmic manifestations in patients of sickle cell disease (SCD). Methods : This study was conducted in Acharya Vinoba Bhave Rural Hospital, JN medical College, Wardha. All the patients coming regularly to sickle cell O.P.D for follow up and those who were admitted for sickle cell crisis in medicine ward , obstetrics/gynecology patients who were found to be sickle cell positive (SS pattern) and pediatric patients diagnosed with sickle cell disease were included for this study. A total of 35 sickle cell disease (SCD) patients were studied. Hematologic investigations were done and ophthalmic investigations such as visual acuity, silt lamp bio-microscopy and fundoscopy was done and compared. For statistical analysis SPSS software was used. Results: The study showed that 70% of the Sickle cell disease patients with hemoglobin 6 gm % or less had some ocular abnormality. Conclusion : All sickle cell disease patients should have regular ophthalmic examination to prevent the risk of sickle cell retinopathy. Key words : Sickle cell disease , SS pattern, sickle cell retinopathy I. Introduction In India, haemoglobinopathies have been considered responsible for the largest number of genetic disorders and hence contribute to the imbalance in the health profile of the nation. The cumulative gene frequency of haemoglobinopathies in India is 4.2%. With a population of over 1 billion and a birth rate of 28 per 1000, there are over 42 million carriers and over 12,000 infants are born each year with a major and clinical significant haemoglobinopathy. (4, 5, 6) Despite being characterized by the same point mutation, the clinical course of Sickle Cell Disease (SCD) is extremely variable, ranging from mild to very severe depending on the different genotypes. (7, 8, 9, 10) Painful crisis and severe hemolytic anemia are the two most common systemic complications. However, ocular manifestations are usually mild and asymptomatic. Ocular changes such as conjunctival sickling sign at the conjunctiva (11, 12, 13, 14) and iris atrophy have been noticed. Changes over the other vascular regions of the eye are seen in the choroid, optic disc, and the retina (15) .Though nearly all structures in the eye are affected in Sickle cell disease but, the vision threatening problems are due to retinal neovascularization.(17,18) Sickle cell retinopathy develops in up to 42% of individuals during the second decade of life. (16) A complication of proliferative sickle cell retinopathy (PSCR) is a major contributor for vision loss and visual impairment in 10-20% of affected eyes. (19, 20, 21) Micro-vascular occlusions being the most common cause of visual loss, it is logical then to assume that Sickle cell disease patients who suffer repeated episodes of vasocclusion are vulnerable to visual loss causing blindness. The number of patients who suffer vasocculsive crisis is unclear. The purpose of this study is to document early ocular abnormalities in sickle cell patients and to suggest the need for earlier ophthalmic screening. II. Aims And Objectives To study the ocular pathologies in sickle cell disease and correlate them with hematological parameters.
  • 2. Ocular manifestations in sickle cell disease – A preventable cause of blindness? DOI: 10.9790/0853-141151116 www.iosrjournals.org 12 | Page III. Methodology Site Setting – This was a cross sectional study conducted in Acharya Vinobha Bhave Rural Hospital (A.V.B.R.H), a 909 bedded rural tertiary hospital of Datta Meghe Institute Of Medical Sciences(DMIMS) sawangi(Meghe), Wardha. The study was conducted over a period of 2 months, with due clearance of institutional ethical committee. 1. Study Population – All diagnosed cases of sickle cell disease (by Hb electrophoresis) in AVBRH were examined for ocular manifestations. Sample Size – 36 Inclusion Criteria –  Sickle cell patients who came for regular follow up/admitted for sickle cell crisis. Exclusion Criteria –  Anemias other than sickle cell disease.  Patients with sickle cell trait, sickle cell thalassaemia and other genetic hemoglobinopathies other than sickle cell disease. Procedure/Proposed Intervention  All patients confirmed sickle cell on Hb electrophoresis were included in this study.  Complete blood counts , Hemoglobin, red cell indices, white cell count and platelet count were done.  Detailed ocular examination as follows: assessment of visual acuity using Snellen‘s chart. Anterior segment structure viz conjunctiva, cornea, iris and lens was examined using silt lamp examination.  Indirect ophthalmoscopy were carried out for lesions in posterior segment.20 D lens was used to examine the peripheral retina.  Fundus examination with binocular indirect ophthalmoscope and silt lamp biomicroscopy.78 D and 90 D lens was used in silt lamp biomicroscopy to examine optic disc changes and macular changes.  Color photographs by fundus camera and fluorescien angiography (FFA) were done in cases with suspected proliferative sickle retinopathy. Goldberg classification was followed for classifying sickle cell retinopathy if present. Statistical Analysis SPSS software was used for statistically analyzing the collected data and results obtained will be interpreted in the form of tables, graphs and charts. IV. Observations And Results Table 1: Comparison of parameters in positive and negative patients Student‘s unpaired t test N Mean Std. Deviation Std. Error Mean t-value p-value Hb% Positive 7 4.00 0.42 0.16 5.38 0.0001,S,p<0.05 Negative 28 8.55 2.20 0.41 Total RBC Positive 7 1.91 0.77 0.29 4.50 0.0001,S,p<0.05 Negative 28 3.44 0.81 0.15 RDW Positive 7 26.40 2.01 0.76 10.63 0.0001,S,p<0.05 Negative 28 17.13 2.07 0.39 Total WBC Positive 7 2857.14 468.53 177.08 3.79 0.001,S,p<0.05 Negative 28 7646.42 3297.64 623.19 MCV Positive 7 91.28 4.85 1.83 5.27 0.0001,S,p<0.05 Negative 28 72.57 8.99 1.69 MCH Positive 7 28.82 2.84 1.07 0.29 0.76,NS,p>0.05 Negative 28 28.34 4.05 0.76 MCHC Positive 7 33.28 1.66 0.63 0.54 0.58,NS,p>0.05 Negative 28 32.791 2.22 0.42 Platelet Count Positive 6 1.69 0.11 0.04 2.79 0.009,S,p<0.05 Negative 27 3.00 1.13 0.21
  • 3. Ocular manifestations in sickle cell disease – A preventable cause of blindness? DOI: 10.9790/0853-141151116 www.iosrjournals.org 13 | Page Table 2: Correlation of Hb% with other clinical parameters Pearson‘s Correlation Coefficient Parameters Mean Std. Deviation N Correlation ‗r‘ p-value Hb% 7.64 2.70 35 - - Total RBC 3.14 1.00 35 0.64 0.001,S RDW 18.99 4.27 35 -0.50 0.002,S Total WBC 6688.57 3528.77 35 0.40 0.014,S MCV 76.31 11.22 35 -0.53 0.001,S MCH 28.44 3.81 35 -0.12 0.45,NS MCHC 32.89 2.11 35 0.12 0.48,NS Platelet Count 2.76 1.14 33 0.50 0.003,S
  • 4. Ocular manifestations in sickle cell disease – A preventable cause of blindness? DOI: 10.9790/0853-141151116 www.iosrjournals.org 14 | Page Table 3: Ocular Incidence According To Hemoglobin Concentration Hemoglobin Range Sickle Cell Disease Total Cases No. with Ocular Changes % Less than 6 gm% (Severe) 10 7 70 6 – 10 gm% (Moderate) 18 0 0 10 – 13 gm% (Mild) 8 0 0 Above 13 gm% 0 0 0 Table 4: Ocular Manifestations Ocular Manifestations Fundus in General Sickle Cell Disease No. of Cases with Ocular changes n = 7 % Major retinal vessel changes 2 28.57 Hemorrhages in periphery 4 57.14 Neovascularisation 1 14.28 Iridescent glistening vessels - 0 Peripheral vessel deposits - 0 Chorioditis - 0 V. Discussion Sickle cell haemoglobinopathy is a common disorder of this area. Irrespective of any ocular complaints, a search was made for ocular changes amongst the 36 sickle positive patients. Despite the fact that none of them had any ocular symptoms, but various ocular signs were found in them. All the patients except one who had been admitted for vision defect and was found to have neovascularisation. Out of the 36 sickle positive patients, 26 cases (72.22%) were below 30 years of age, the youngest patient being 7 years old. There was one case of sickle cell anemia after 40 years. Seventeen patients were male and 19 were of the females (57.16%). Females were more affected than males. Goldberg et al and Condon et al had also observed such sex predilection in their cases. The caste distribution was majority were from religion buddha (61.11%), Teli (27.77%), goud (11.11%). It should be noted that 70% of the Sickle cell patients were found with less that hemoglobin 6 gm % had some ocular changes. Pallor, icterus and vascular changes (90.47%) were observed in the conjunctiva. The vascular changes were of grade I and consisted of comma shaped or cork screw shaped or abnormally long, linear dilatations of vessels still connected to the vascular network with sludged flow, mostly observed in the bulbar conjunctiva covered by lids. Kate et a1and Condon et al (97.4% in Hb-SS cases) have observed such changes in various degree in sickle cell anemia and sickle cell Hb-C disease other than sickle cell trait. Significant changes were observed in major retinal vessels (28.57%). The major retinal vessels were dilated, full and tortuous, the veins being more tortuous than arteries. In some cases, the arteries were pale and narrow. The peripheral vessels were tortuous and sometimes occluded, but in a few cases, the arterioles were chalky white in color, associated with perivascular sheathing, occlusion and tortuosity.
  • 5. Ocular manifestations in sickle cell disease – A preventable cause of blindness? DOI: 10.9790/0853-141151116 www.iosrjournals.org 15 | Page Similar findings have been documented by Condon et al, who found peripheral vessel disease 93.4% and major retinal vessel changes in 10.5% of Hb. SS cases; whereas Kate et a1have found venous fullness and venous tortuosity in 18% and 24% of their series. Hemorrhage (57.14%) and neovascularisation (14.28%) were also observed in the peripheral retina. Condon et al; had noted retinal hemorrhage (2.6%) and tortuosity and dilatations of capillary network with micro-aneurysmal formation and neovascularisation (39.5%) in the Hb-SS cases of his study, but Kate et al did not get any case of retinal hemorrhage in their series (instead they had observed vitreous hemorrhage in one case). Majority of cases with ocular involvement in all categories of haemoglobinopathies were within the third decades of life although highest incidence occurred in the second decade as observed in this study. Goldberg et al had observed the mean age for the ocular changes as 28 years, while Condon et al had seen maximum changes in 10-20 years. His study in Jamaica in elderly age groupsshowed that incidence of peripheral vessel disease appears to increase with age. Majority of cases of different haemoglobinopathies had ocular changes in moderate and severe degree of anemia (less than 6 gm. % of hemoglobin). But the comparison of the prevalence of ocular changes in different hemoglobin concentrations and in various haemoglobinopathies, of this study, indicates that besides anemia, the abnormal sickle hemoglobin is the prime cause for the ocular changes in this disorder (e.g. in 6-10 gm.% of hemoglobin range, indicating that simple anemia is not the only cause). VI. Conclusion Sickle cell disease is a disease of national concern. Its complication continue to remain as a significant issue to physicians. Visual loss which occurs due to vasocculsive crises can be prevented in patients of sickle cell disease by early ocular diagnosis as it would seem, logical to assume that patients with SCD who suffer from repeated episodes of vaso-occlussion might be most vulnerable to ocular pathology. Therefore, this study attempts to include ocular examination in routine investigation of sickle cell tests and in routine follow up check-ups in diagnosed cases of sickle cell disease. Thus, protecting them from visual impairment and visual loss. References [1]. Balgir RS 1996. The prevalence of sickle cell haemog-lobinopathy in India. In: TheEncyclopedia of Dravidian Tribes. Vol. 1 T.Madhava Menon, C Siva Thanu, K.P.Prasanth, M. Sasikumar and PRG Mathur (Eds.). Trivandrum: The International School of Dravidian Linguistics pp 21-29. [2]. Bhatia HM, RaoVR 1987. 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