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SHORT COMMUNICATION
Year : 2006  |  Volume : 12  |  Issue : 2  |  Page : 86-92
 

Genetic heterogeneity of population structure in 15 major scheduled tribes in central-eastern India: A study of immuno-hematological disorders


Division of Human Genetics, Regional Medical Research Center (ICMR), Chandrasekharpur, Bhubaneswar, Orissa, India

Correspondence Address:
R S Balgir
Division of Human Genetics, Regional Medical Research Center (ICMR), Opposite Kalinga Hospital, Chandrasekharpur, Bhubaneswar - 751 023, Orissa
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0971-6866.27792

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   Abstract 

Background:0 The aboriginal tribes of India constitute an important segment of the society in the world. Though a large number of genetic studies have been carried out in India, the genetic data of the populations in the state of Orissa are very limited, especially pertaining to the indigenous tribal people. Most of the earlier studies were restricted to either a single tribe or a few genetic markers. Data on population structure of tribal communities of Orissa pertaining to common hemolytic disorders and genetic variations are still scanty. AIMS AND OBJECTIVES: In view of the limited data available on the tribes and the huge tribal population, a cross-section of ashram schools was investigated for immuno-hematological disorders in relation to geographical, linguistic and genetic variations. MATERIALS AND METHODS: A cross-section of 15 major scheduled tribes in ashram schools from eight districts of Orissa was randomly studied for five hereditary immuno-hematological markers, namely, the ABO and Rhesus (D) blood groups, sickle cell hemoglobinopathy, β -thalassemia syndrome and G-6-PD deficiency, following the standard hematological procedures and techniques. RESULTS: A preponderance of blood group B over A and low incidence of Rhesus-negative (D-) among Bathudi, Bhuyan, Kissan, Kolha, Kondh, Munda oraon, Paraja, Santal and Saora tribes was observed. The deficiency of G-6-PD enzyme was found to be quite high, varying from 5.1 to 15.9% among these scheduled tribes of Orissa. Both deficient female heterozygotes and homozygotes were encountered. Marked variation was seen in the prevalence of β -thalassemia trait, varying from 0 to 8.5%, in the aboriginal tribes. The frequency of sickle cell disorders was found to vary from 0 to 22.4% among the major tribes, but it was comparatively higher in Paraja (21.5%), Dhelki Kharia (13.7%), Gond (11.9%) and Bhatra (10.5%) tribes. CONCLUSIONS: The study showed genetic heterogeneity and diversity with respect to above immuno-hematological genetic markers and indicated not only the inter-tribal admixture but also diffusion with other racial groups of India. Further, the heterogeneous tribal populations from Orissa were found to harbor almost all major hemoglobinopathies. This is the first comprehensive study of immuno-hematological disorders among the scheduled tribes from the state of Orissa.


Keywords: b-thalassemia syndrome, ABO and Rhesus blood groups, G-6-PD deficiency, genetic heterogeneity, Orissa, sickle cell disease, tribal populations


How to cite this article:
Balgir R S. Genetic heterogeneity of population structure in 15 major scheduled tribes in central-eastern India: A study of immuno-hematological disorders. Indian J Hum Genet 2006;12:86-92

How to cite this URL:
Balgir R S. Genetic heterogeneity of population structure in 15 major scheduled tribes in central-eastern India: A study of immuno-hematological disorders. Indian J Hum Genet [serial online] 2006 [cited 2015 Aug 1];12:86-92. Available from: http://www.ijhg.com/text.asp?2006/12/2/86/27792


The people of India exhibit a unique range of sociocultural, linguistic, religious, ethnic and biological diversity. Several waves of people of different ethnic stocks, cultures and languages either invaded India or migrated to India from different directions and contributed significantly to the present-day gene pool of the subcontinent.[1],[2] These people not only settled in India but also gradually merged and mingled with the autochthonous local populations. The people of India form thousands of endogamous groups under the broad categories of castes, ethnic groups, tribes and different religious groups. The varied climatic and ecological regime of the country seems to have nurtured this biodiversity. Several anthropological studies based on genetic markers were carried out to understand the genetic variations among the indigenous populations. The blood groups, red cell enzymes and serum proteins were extensively studied among the regional, ethnic and linguistic groups to understand the genetic history, origin and affinities of the Indian populations.[1]-[4]

The autochthonous tribal populations of India live in virtually inaccessible forests and hilly areas completely isolated from the general stream of the society. They have evolved their own morphogenetic characteristics in their respective ecological niches. Tribal communities in Orissa state are highly vulnerable to hereditary diseases and have a high degree of malnutrition, morbidity and mortality. Tribal health is further compounded by poverty, illiteracy, ignorance of causes of diseases, hostile environment, poor sanitation, lack of safe drinking water, faith in traditional beliefs, exploitation by elites, etc. The state of Orissa ranks third in terms of tribal population in India. They constituted 10.84% of the total tribal population of India as per 2001 census.

Among the several hereditary disorders of blood, hemoglobinopathies, glucose - 6 - phosphate dehydrogenase (G-6-PD) enzyme deficiency and blood group serology are the most important genetic and public health issues in the state of Orissa. Though a large number of genetic studies have been carried out elsewhere among the tribes in India,[1],[2],[3],[4],[5] the genetic data of the populations in the state of Orissa are very limited, especially pertaining to the indigenous tribal people. Most of the earlier studies were restricted to either a single tribe or a few genetic markers and were mainly descriptive rather than analytical in nature. ABO blood groups are the most extensively studied genetic system in Orissa.[1],[3],[4] Further, the previous studies were either hospital based[6] or without following any systematic sampling procedure.[1] Hence the data on the exact magnitude of hemoglobinopathy and allied genetic disorders are lacking. Data on population structure of tribal communities of Orissa pertaining to common hemolytic disorders and genetic variations are still scanty.

In view of the limited data available on the tribes and the huge tribal population practicing clan exogamy and tribe endogamy and matrimonial hindrance caused by natural physical barriers in the state, a cross-section of ashram schools belonging to 15 major scheduled tribes of Orissa was investigated for some common serogenetic markers and hereditary hematological disorders. The present study aims at a comprehensive analyses of population structure in relation to geographical, linguistic and genetic variations.


   Materials and Methods Top


Out of the 62 scheduled tribes in the state, which comprised 22.4% of the population of Orissa, 15 major tribes were selected for this study, based on their total population in the state, the criterion being a population of more than one lakh of each tribe as per 2001 census. The major tribes included were Bathudi, Bhumiz, Kolha, Lodha and Santal from Mayurbhanj district; Bhuyan, Kharia, Kissan, Munda and Oraon from Sundargarh district; Bhatra from Nawarangpur district; Gond from Kalahandi district; Kondh from Kandhamal (Phulbani) district; Paraja from Koraput district; and Saora from Ganjam and Gajapati districts in the central-eastern part of India [Figure - 1]. A tribe acquires the 'primitive tribe' status based on diminishing or stagnant population, low level of literacy, pre-agricultural level of technology, seclusion from mainstream, social isolation and archaic mode of life. There are 12 primitive tribes in Orissa, namely, Birhor, Bonda, Didayi, Dongria Kondh, Hill Bhuyan, Hill Kharia, Juang, Kutia Kondh, Lanjia Saora, Lodha, Mankirdia and Saora.

The tribes in Orissa, as in the whole of India, are by no means homogeneous in their history, language, culture or social organization. It may be mentioned here that the major tribes of Orissa belong to three linguistic groups, namely, Indo-Aryan or Indo-Europeans (Non-Australoid), Austro-Asiatic (Mundari) speakers (Proto-Australoid) and Dravidian (Gondi or Kuvi) speakers (Australoid). Mundari speakers (Austro-Asiatic) belong to Proto-Australoid racial group, which include Bhumiz, Gadaba, Juang, Kharia, Koda, Kolha, Mahali, Mirdha, Munda, Santal and Saora tribes. The Northern Mundari comprise of tribes such as the Bhumiz, Juang, Kharia, Kolha or Ho, Korku, Munda and Santal; and from the southern region, the Southern Mundari covering the tribes, namely, Bonda, Didayi, Gadaba, Parenga and Saora. Tribes like Bathudi, Bhatra, Binjhal, Bhuyan, Lodha and Saunti are Indo-Aryan or Indo-European speakers and belong to non-Australoid racial stock. The Dravidian (Kuvi or Gondi) speaker group belongs to Australoid racial stock and includes Gond, Kondh, Kissan oraon, Paraja and Pentia Halva tribes.

The districts with higher concentration were first identified for each tribe and then the ashram schools were listed in that locality. Out of several ashram schools so listed, 4-5 ashram schools were selected at random, representing different geographical locations in each district from eight districts of the state [Figure - 1]. A total of 1,959 blood samples of children from ashram schools were collected after taking informed consent from each individual during the period 1995-2000. It was also ensured that blood samples were collected from unrelated individuals belonging to either sex.

About 2-3 ml of intravenous blood was collected from each student under aseptic conditions in ethylene diamine tetra acetic acid (EDTA) coated vials after obtaining informed consent. The ABO and Rhesus (D) blood groups' typing was done in the field and the rest of the blood samples were transported under ice-cold conditions to the laboratory at Bhubaneswar within 24 h of collection and were analyzed using standard procedures. ABO and Rhesus blood groups' typing was done by slide method, following the instructions of the manufacturer (Tulip Diagnostics Private Limited, Goa). The sickling test was performed by wet sealed method, using 2% freshly prepared sodium metabisulphite solution, following the methodology of Dacie and Lewis.[7]

Further, hemoglobin (Hb) electrophoresis was performed on cellulose acetate membrane, and fraction of hemoglobin A 2 was estimated by elution method using Tris-EDTA-Borate (TEB) buffer at pH 8.9[7],[8] and fetal hemoglobin as per standard procedures.[8] The hemoglobin A 2 value of more than 3.5% was taken as the cut off point for β -thalassemia trait. The glucose-6-phosphate dehydrogenase (G-6-PD) enzyme deficiency was detected by using dichlorophenol Indophenol dye, as described by Bernstein[9] and subsequently confirmed by WHO procedures[10] and Beutler and co-workers.[11] The allele frequencies for each system, i.e., ABO and Rhesus blood groups, sickle cell, β -thalassemia and G-6-PD deficiency, were estimated as per standard guidelines and procedures.[12]


   Results Top


[Table - 1] shows the distribution of sickle cell disorders (sickle cell trait and disease), which varied from 0 to 22% among the 15 major tribes of Orissa. High frequency of sickle cell disorders was observed among the Gond (22.4%), Bhatra (18.1%), Paraja (14.8%), Kharia (7.4%) and Saora (7.3%) tribes. The frequency of sickle cell trait was higher than the sickle cell disease. Sickle cell disorders were found absent among Bhuyan, Kissan, Kolha, Lodha and Oraon tribes. The distribution of β -thalassemia trait showed a wide range of variations, viz., from 0 to 8.5% among the major tribes of Orissa. High incidence of β -thalassemia trait was noted among Paraja (8.5%), Santal (8.0%), Lodha (6.7%), Bhatra (6.6%), Kondh (6.3%), Saora (6.2%) and so on in decreasing order. However, no case of sickle cell β -thalassemia was detected in the present study.

It is apparent from [Table - 1] that the distribution of G-6-PD deficiency among the 15 major tribes of Orissa was quite high and varied from 5.1 to 15.9%. The frequency of this enzyme deficiency was high in males (range 4.3-17.4%) than in females (range 0-13.6%). Both deficient female heterozygotes and homozygotes were encountered. High frequency of G-6-PD deficiency was observed among Munda (15.9%), Paraja (15.9%), Kharia (14.2%), Bhuyan (12.9%), Kolha (9.8%), Bathudi (9.5%), Bhumiz (9.5%), Santal (9.0%) and Oraon (8.2%) tribes.

The frequency of blood group B showed preponderance over that of blood group A among Bathudi, Bhuyan, Kissan, Kolha, Kondh, Munda oraon, Paraja, Santal and Saora tribes but not among Bhumiz, Gond, Kharia and Lodha tribe, thereby showing their ethnic diversity. High frequency of blood group O was observed among Bhatra (39.8%), Gond (38.4%), Kissan (32.3%), Santal (32.0%) and Bhumiz (31.0%) tribes. The frequency of Rhesus-negative (D-) was very low (range 0 to 2.1%) among the 15 major tribes of Orissa. The Rhesus blood group (D-) was found to be completely absent among Bhumiz, Kharia, Kissan, Kolha, Lodha, Munda, Paraja, Santal and Saora tribes.

[Table - 2] shows the allele frequency data of the various systems studied here. It is apparent from the table that the frequency of sickle cell allele varied from 0 to 12% among the major tribes of Orissa. β -thalassemia was not very common (range 0-4%) among the tribes. Highest frequency of G-6-PD deficiency allele (Gd-) was observed among the Parajas (13.4%) of Koraput district of Orissa. Of the ABO blood group systems, most commonly observed allele was blood group B among the tribes. The allele for Rhesus negative (D-) blood group varied from 0 to 14.5% among the major tribes of Orissa [Table - 2].


   Discussion Top


The autochthonous scheduled tribes are by no means homogeneous in their history, language, culture or social organization in India. From an ethnographic point of view, central-eastern India has been the home of many aboriginal tribes inhabiting virtually inaccessible interior hill and forest environments that generally inhibited gene flow among the tribal groups. Since early times, the aboriginal tribal groups have been living in near isolation and have evolved their own morphogenetic characteristics in their respective ecological niches. The net effect has been the creation of multiple genetic isolates, accentuation of certain recessive alleles, ignoring the clinical consequences of this highly complex differentiation, leading to population heterogeneity and genetic diversity.

This is the first comprehensive immuno-hematological study on scheduled tribes from Orissa. The most striking feature that emerged from the present study was the genetic admixture in almost all the genetic parameters studied here. This is apparent in the distribution of hereditary hematological disorders like sickle cell disease, β -thalassemia or G-6-PD deficiency, as well as in the allelic frequencies of serological characters like ABO and Rhesus blood groups among these tribes. This admixture may be due to pressures of gene diffusion from different waves of people who penetrated their habitats and territory in course of invasions and migrations from the northwestern (Indo-Aryan) and northeastern (Mongoloid) parts of the country since time immemorial. Both linguistic and racial admixtures have occurred among the major tribes that manifested genetic heterogeneity and diversity with respect to mongoloid, australoid, proto-australoid and nonaustraloid characteristics in the state of Orissa.

A preponderance of blood group A over the B allelic frequency has been observed among Bhumiz, Gadaba, Kharia and Saora (proto-australoid tribes); Gond, Kondh and Paraja (australoid tribes); Bhatra and Lodha (nonaustraloid tribes); which is a characteristic feature of Mongoloid populations in the northeastern part of India[2] [Table - 2]. Similarly, the allelic frequency of Rhesus blood group D- is low among the northeastern (Mongoloid) populations of India.[2] Almost all the major tribes of Orissa have shown a reduced frequency or complete absence of D- allele, except among Bathudi, Bhuyan, Oraon (in the present study) and Saora tribe (studied by Mishra).[3] The Rhesus-negative (D-) blood group even was found completely absent among some tribes like Bhumiz, Kharia, Kissan, Kolha, Lodha, Munda, Paraja, Pentia Halva and Saora [Table - 2]. This supports the findings of admixture of major tribes of Orissa with that of Mongoloid elements of northeastern India. Further, there is a marked intra-tribal fluctuation in the ABO and Rhesus allele frequencies studied by various researchers in Mundari speakers of northern and southern Orissa, Dravidian or Kuvi speakers, as well as Indo-Aryan or Indo-European speaker tribes [Table - 2], indicative of genetic heterogeneity. For the first time, two unrelated cases of Bombay (Oh) phenotype were detected in Kutia Kondh primitive tribe from Belghar area of Kandhamal (Phulbani) district in Orissa and reported elsewhere.[13]

The G-6-PD enzyme deficiency is clinically the most prevalent significant disorder in man and is one of the etiological factors associated with severe neonatal jaundice in full-term normal weight infants in India.[14] The distribution of this x-linked enzyme deficiency among the major tribes of Orissa is interesting. There is a high degree of variation in the frequency of G-6-PD enzyme deficiency in almost all the major tribes of Orissa [Table - 1]. The deficient allele frequency is the highest in Mundari speakers (7.4-30.7%) of northern Orissa, followed by Indo-Aryans (2.8-21.1%) and Dravidians (2.9-13.4%). The lowest frequency of the deficient allele was observed among Mundari speakers of southern Orissa. High frequencies of this enzyme deficiency have been observed among some populations like Warli (17.0%), Parsis (15.7%), Madia (14.4%), etc., in western India[15]; and Mongoloid tribal populations like Angami Naga (27.0%), Adi (19.4%), Apatani (16.7%), Nishi (16.0%), Rabha (15.8%), Mikir (15.6%), etc.,[2],[14] in northeastern India. The high frequency of deficient enzyme among the major tribes of Orissa, especially among Bathudi, Bhuyan, Juang, Kolha, Munda, Paraja and Santal tribes [Table - 1], further testifies the contention of diffusion and gene flow of Mongoloid elements among the tribes of Orissa. Further, it is interesting to note that the frequency of G-6-PD deficiency is equally high among the Austro-Asiatic and Indo-Aryan speakers [Table - 1].

The most likely explanation for this situation is that the Austro-Asiatic speakers, whose ancestors probably came to central India or southern Orissa during prehistoric times and brought this deficient allele with them later through the process of admixture, spread due to founder effect into the populations speaking Dravidian and Indo-Aryan languages. However, the genetic drift due to the founder effect and relative isolation is clearly seen in Mundari speakers (Bondo, Didayi and Saora tribes) of southern Orissa for this trait [Table - 1]. The allele frequency of deficient enzyme is low (2.9-8.9%) among the Dravidian tribes (Gond, Kondh, Kissan and Oraon) except the Paraja tribe (13.4%) of Orissa.

Recently, the G-6-PD enzyme deficiency among the tribes (including the tribes involved in the present study, like Bathudi, Bhuyan, Munda and Santal) of India has been identified a new variant, called 'G-6-PD Orissa,' which has more or less 10-20% of the normal enzyme activity and normal electrophoretic mobility but has a five-fold higher Michael's constant (KmNADP) for the substrates, which actually translates roughly into five-fold lower activity at limiting substrate concentrations and shows increased thermostability than normal enzyme.[16] This implies that the antimalarial drugs like primaquine and many other compounds such as phenacetin, furadantin, certain sulphonamides and acetyl salicylic acid (aspirin), etc., should be administered with caution among the major tribes of Orissa, which may cause hemolytic crisis and sometimes be fatal also.

Certain genetic systems such as hemoglobin polymorphism show spatial patterning, which may reflect adaptation to a corresponding environmental variable(s). Though the frequency of sickle cell allele varies from 0 to 21.5% among the various tribes of Orissa [Table - 1], depending upon the economy, sociocultural and reproductive practices, it is comparatively higher in Paraja (21.5%), Gond (11.9%) and Bhatra (10.5%) tribes. The allele frequency of sickle cell is very low among the Austro-Asiatic speakers (0-4.8%), except Dhelki Kharia in Orissa. The Bhatra tribe speaks Indo-Aryan, and the Gond and Paraja are Dravidian tribes. This shows that the sickle cell allele, which was probably prevalent initially in the Dravidian populations, has now penetrated the Indo-Aryan populations or vice versa and indicates the genetic admixture among these populations. Further support to these findings has come from studies of the origin of sickle cell gene in India.[3] The sickle cell gene was found absent among the Bhuyan, Kissan, Kolha, Lodha and Oraon tribes in the present study, reflecting their genetic isolation from the rest of the surrounding populations, among whom the sickle cell gene is commonly encountered.

It is surprising that the heterogeneous tribal population is harboring almost all major hemoglobinopathies in Orissa. A family with hemoglobin D trait was encountered in Paik Bhuyan tribe from Orissa.[15] Hemoglobin E gene was detected in heterozygous and homozygous form in Dhelki Kharia tribe for the first time in Sundargarh district of Orissa.[15] A family with hereditary persistence of fetal hemoglobin (HPFH) was detected for the first time in Paraja Bhuyan tribe and described elsewhere.[15]

Further, the state of Orissa is highly endemic for malaria, especially for Plasmodium falciparum , which takes a high toll of lives in the state every year. The state of Orissa, which constitutes 4% of the population of India, contributes 22% of malaria cases, with 83% of these being Plasmodium falciparum cases - 50% of which lead to deaths . The individuals with this enzyme deficiency have an advantage over the nondeficient persons that the malarial parasites do not survive for longer duration in these individuals and die due to lack of favorable bio-environment. Hence the deficient individuals in malarial endemic bio-environment do not suffer severely from malaria; rather they have adapted themselves to this kind of bio-environment and have developed to some extent immunity against it. This is evident from the fact that some individuals do not manifest clinical symptomatology although they carry the malarial parasite in their blood.

It is interesting that the distribution of sickle cell (Hb S) and β -thalassemia allele frequencies showed that when Hb S is depressed, the β -thalassemia allele is elevated [Table - 1]. Whether the frequency clines of these two alleles represent gene flow across the region or provide a compensatory selective mechanism against malaria is worth exploring. The findings of the present study indicate the possibility of the gene flow across the tribes as well as of the existence of selective mechanism against malaria in Orissa. The frequency of β -thalassemia allele is very high among the major tribes (range 0-5.4%) of Orissa [Table - 2].

Various factors of population structure - such as population size, density, mating pattern; and micro-evolutionary forces like differential selection, migration, etc., considerably contribute to the diversity within the population. The present analysis indicates that, in addition to genetic drift, gene flow and selection, the genetic structure of the tribal populations of Orissa is highly influenced by economy, sociocultural adaptation and inbreeding. Further, although some of the variations may be due to the sample size, number of tribes, geographic distance between tribal populations, variables tested and breeding structure of the population, the present analysis strongly suggests that the infrastructure of these tribal populations is highly influenced by the local inbreeding within each tribal population. These findings get further support from Balgir.[3]


   Conclusions Top


Autochthonous tribal communities constitute an important segment of the society in India. They are highly vulnerable to hereditary hemolytic disorders and have a high degree of morbidity and mortality affecting their health and quality of life, particularly in Orissa. Both linguistic and racial admixtures have occurred among the major scheduled tribes who manifest genetic heterogeneity and diversity with respect to the five genetic markers in Orissa. This may be due to continuous pressures of gene diffusion from different waves of people penetrating their habitats and territory in course of invasions and migrations from the northwestern (Indo-Aryan) and northeastern (Mongoloid people) parts of India during ancient and historical times. In addition to the above, inter-linguistic, inter-racial and inter-tribal admixture, and sometimes intra-tribal isolation, has also occurred as reflected by the genetic parameters studied here. There is a strong evidence for the operation of a compensatory selective mechanism against malaria by way of high prevalence of the sickle cell, β -thalassemia and G-6-PD deficiency among the tribes of Orissa. Further, the heterogeneous tribal population is harboring almost all major hemoglobinopathies like Hb D, E and HPFH apart from those of the present study in Orissa. This is the first comprehensive study of immuno-hematological disorders among the scheduled tribes from the state of Orissa.


   Acknowledgments Top


The author is grateful to Dr. S. K. Kar, Director of this center, for providing the necessary facilities to carry out the study. My heartfelt thanks go to District Welfare Officers, Headmasters, Teachers and ashram school students of all the concerned districts for their cooperation and help during the collection of data. Thanks are also due to Mr. R. K. Mishra, Lab. Tech., for his field and laboratory support.

 
   References Top

1.Papiha SS, Roberts DF, Mishra SC. Serogenetic studies among an urban and two tribal populations of Orissa, India. Ann Hum Biol 1988;15:143-52.  Back to cited text no. 1  [PUBMED]  
2.Balgir RS. Emerging trends in genetic epidemiology of hemoglobinopathy in the seven sister states of North Eastern India. In : Das Rajat Kanti, Basu Debashish, editors. North East India in Perspectives: Biology, Social Formation and Contemporary Problems. Akansha Publishing House: New Delhi; 2005. p. 17-37.   Back to cited text no. 2    
3.Balgir RS. Human genetics, health and tribal development in Orissa. In : Dash Sharma P, editor. Environment, health and development: An anthropological perspective. S. C. Roy Institute of Anthropological Studies: Ranchi; 2000. p. 87-104.  Back to cited text no. 3    
4.Bhasin MK, Walter H. Genetics of castes and tribes of India. Kamla-Raj Enterprises: Delhi; 2001. p. 58-89.  Back to cited text no. 4    
5.Bhatia HM, Rao VR. Genetic atlas of Indian Tribes. Institute of Immunohematology (ICMR): Mumbai; 1991.   Back to cited text no. 5    
6.Kar BC. Sickle cell disease in India. J Assoc Physics India 1991;39:954-60.  Back to cited text no. 6  [PUBMED]  
7.Dacie JV, Lewis SM. Practical Hematology. 7th ed. Churchill Livingstone: Edinburg; 1991. p. 227-57.  Back to cited text no. 7    
8.Weatherall DJ. Hematologic methods. In : Weatherall DJ, editor. Methods in Hematology: Thalassemias. Vol. 6. Churchill Livingstone: New York; 1983. p. 27-53.  Back to cited text no. 8    
9.Bernstein RE. A rapid screening dye test for detection of G-6-PD deficiency in red cells. Nature 1962;194:192-3.  Back to cited text no. 9  [PUBMED]  
10.Standardization of procedures for study of glucose-6-phosphate dehydrogenase. Report of a WHO Scientific Group. World Health Organ Tech Rep Ser 1967;366:1-53.  Back to cited text no. 10    
11.Beutler E, Blune EG, Kaplan JC, Lohr GW, Ramot B, Valentine WW. International committee for standardization in hematology recommended screening test for glucose-6-phosphate dehydrogenase deficiency. Br J Hematol 1979;43:465-7.  Back to cited text no. 11    
12.Mourant AE, Kopec AC, Domaniewska-Sobczak K. The distribution of the human blood groups and other polymorphisms. Oxford University Press: London; 1976. p. 47-61.  Back to cited text no. 12    
13.Balgir RS. Detection of a rare "Bombay (Oh) Phenotype" among the Kutia Kondh primitive tribe of Orissa, India. Int J Hum Genet 2005;5:193-8.  Back to cited text no. 13    
14.Balgir RS. Ethnic and regional variations in the red cell glucose-6-phosphate dehydrogenase deficiency in India. Indian J Hemat 1989;7:101-9.  Back to cited text no. 14    
15.Balgir RS. The spectrum of hemoglobin variants in two scheduled tribes of Sundargarh district in North-Western Orissa, India. Ann Hum Biol 2005;32:560-73.  Back to cited text no. 15  [PUBMED]  
16.Kaeda JS, Chhotray GP, Ranjit MR, Bautista JM, Reddy PH, Stevens D, et al . A new glucose-6-phosphate dehydrogenase variant, G6PD Orissa (44 Ala > Gly), is the major polymorphic variant in tribal populations in India. Am J Hum Genet 1995;57:1335-41.  Back to cited text no. 16    


    Figures

[Figure - 1]

    Tables

[Table - 1], [Table - 2]


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