Prevalence of hemoglobinopathies among Malayali tribes of Jawadhu hills, Tiruvannamalai district, Tamil Nadu, India: a community-based cross-sectional study

ABSTRACT

Background

Hemoglobin (Hb), a red pigment of red blood cells (RBCs), carries oxygen from the lungs to different organs of the body and transports carbon dioxide back to the lungs. Any fault present in the Hb structure leads to undesirable functional effects of the RBCs, such as sickle cell anemia (SCA), thalassemia, etc. Hemoglobinopathies affect around 7% of people in both developed and developing countries globally. The aim of the present study was to determine the prevalence and carrier frequencies of hemoglobinopathies including SCA, thalassemia, and other abnormal Hb variants among Malayali tribes in the Jawadhu hills of Tiruvannamalai district, Tamil Nadu, India.

Methods

A community-based cross-sectional study was carried out among 443 Malayali tribes inhabiting the Jawadhu hills of Tiruvannamalai district from July 2022 to September 2022. The RBC indices were analyzed using an automated 5-part hematology analyzer (Mindray, BC-5150) and hemoglobin fractions were done using the HPLC system (Bio-Rad, D-10) following standard protocols.

Findings

A total of 443 participants were screened, out of whom 14.67% had an abnormal Hb fraction, 83.30% were identified as normal, and 2.03% were borderline. Notably, the study revealed a prevalence of 0.68% for the α-thalassemia trait and 13.99% for the β-thalassemia trait.

Interpretation

Haemoglobinopathies, specifically the β-thalassemia trait, were most prevalent among the Malayali tribal population of Tamil Nadu residing in the Jawadhu hills of Tiruvannamalai district. Hence, we need special attention for creating awareness, increasing hemoglobinopathies screening programs, and improving the importance of tribal health conditions by the government and non-governmental organizations (NGOs) for the betterment of the ethnic tribes.

KEYWORDS:

• Hemoglobinopathies
• thalassemia
• Malayali tribes
• Jawadhu Hills
• Tamil Nadu
• India

Introduction

Hemoglobinopathies are a major public health problem among millions of people around the world [1]. The WHO reported that 7% of the world's populations are carriers of hemoglobin (Hb) disorders [2]. Every year, there are over 42 million carriers and more than 12,000 infants born with a major and clinically significant hemoglobinopathy. In India, the cumulative gene frequency of hemoglobinopathies is 4.2% [3]. It is a serious concern from India's community health perspective as well [4–6]. Particularly, Indian tribal or indigenous populations with a high disease burden of sickle cell anemia and thalassemia are most vulnerable [7].

Sickle cell anemia (SCA) is a condition of hemoglobinopathy, which is an autosomal recessive hereditary disease caused by the inheritance of mutant Hb genes [8]. Several researchers in India have reported the presence of sickle cell trait in different Indian tribal groups that are largely confined to their hinterlands, such as northeast, central, and east India, Gujarat, Maharashtra, Kerala, and Tamil Nadu [9–15]. As per the 2011 census, there are approximately 1.8 crore sickle cell gene carriers with approximately 14 lakh patients in India [16].

Thalassemia is a group of genetic diseases wherein the amount of production of α and β-globin chains decreases due to increased destruction in the bone marrow and peripheral blood [17]. If α-globin chains are not formed in sufficient quantities, there will be an increased level of β-globin chains (α-thalassemia); if β-globin chains are insufficiently synthesized, then α-globin chain production will go high (β-thalassemia) [18]. It is estimated that there are 30–40 million carriers, and 8,000–10,000 thalassemics are born every year in India [19]. In India, β-thalassemia is prevalent, with an average frequency of carriers of 3–4% [20], while α-thalassemia is widespread, with a prevalence of 10–25% [21,22].

India has the largest and one of the most diverse tribal populations in the world [23,24]. Tamil Nadu (TN), a southern state of India with 36 types of tribal groups, reports one of the most diverse tribal population landscapes in India [16]. According to the 2011 census, 794,697 Scheduled Tribes (STs) were living in TN, of which 401,068 were male and 393,629 were female. The rural and urban population of ST is 660,280 and 134,417, respectively, and the percentage of the ST population in TN is 1.1% of the total population [25].

Despite the high prevalence of hemoglobinopathies in TN, there has been limited comprehensive research on the prevalence among tribal populations. Importantly, there are no reports available on the prevalence of hemoglobinopathies among Malayali tribes in Tiruvannamalai district. Therefore, the objective of the present study was to identify the prevalence and carrier frequencies of hemoglobinopathies among Malayali tribes in Jawadhu Hills, Tiruvannamalai district, Tamil Nadu, India.

Materials and methods

Ethical consideration

The study was approved by the Scientific Advisory Committee (SAC) and Institutional Human Ethics Committee (IHEC) of ICMR-National Institute of Epidemiology (ICMR-NIE), Chennai (NIE/IHEC/201901-02). Necessary approvals were also taken from the Directorate of Public Health and Preventive Medicine (DPH&PM), the Principal Chief Conservator of Forests (PCCF), the District Forest Office (DFO), the Tribal Welfare Department (TWD) and the District Collectorate (DC). Before the data/sample collection, written informed consent/assent was obtained from adult individuals/adolescents and parents/guardians in the case of minors.

Study design

A community-based cross-sectional study was carried out between July 2022 to September 2022. A total of 443 samples were collected from the Malayali tribes with ages ranging from 6 months to 35 years from both genders. Before the initiation of the field survey, a Community Advisory Board (CAB) committee was formed with representation from the panchayat leaders, tribal heads, tribal village representatives, local panchayat representatives, councilors, village health nurses, etc. Our research team explains in detail the importance and purpose of the study to the CAB committee for their valuable input. After getting confirmation of their availability and willingness to participate in the study with their eligible family members, the field survey was planned and executed.

Study population

Malayali (malai = hills; ali = inhabitants) is one of the 36 STs of TN. As per the 2011 census, 357,980 Malayali tribes were living in TN, of which 181,704 were male and 176,276 were female, and the percentage of the Malayali tribe is 45.05% of the total ST population of TN [16]. The Malayali tribes are spread along the contiguous hill ranges of Jawadhu, Kolli, Yercaud, and Pachamalai; among them, Jawadhu hills are mainly occupied by Malayali tribes (98%) and others (2%). The Malayalis call themselves malaikaran, and male gounders, and also believe that they originally belonged to the Vellala caste of cultivators. Some findings reported that the tribes migrated from the sacred city of Kanchipuram to the hills of southwest TN a few generations ago [26–28].

Study settings

Jawadhu Hills are located in the Eastern Ghats, spread over large areas in the Tiruvannamalai district of TN. The Jawadhu Hills cover an area of 50 miles (80 km) wide and 20 miles (32 km) long. It is bisected into western and eastern parts by three major rivers, viz., Cheyyar, Agaram, and Palar. The altitude of the Jawadhu hills ranges from 1,100–1,150 m higher than the sea level [29]. Study areas of the Jawadhu Hills block, Tiruvannamalai district, Tamil Nadu state, India are shown in Figure 1.

Figure 1. Study area of the Jawadhu Hills block, Tiruvannamalai district, Tamil Nadu state, India. 1. Marganur, 2. Kanaganeri, 3. Kelur, 4. Melnellimarathur, 5. Erimamarathur, 6. Erinellimarathur, 7. Gundalathur, 8. Thekkumarathur, 9. Kilvilamuchi, 10. Athipattu.

Data collection and analysis

The socio-demographic details of the selected tribes were recorded using a standardized questionnaire. About 5 mL of intravenous blood samples were collected in an EDTA containing vacutainer from each of the eligible participants. The RBC indices were undertaken using an automated 5-part hematology analyzer (Mindray, BC-5150). The hemoglobin fractions were identified using the HPLC system (Bio-Rad, D-10) following standard protocols. HbA2 value is a main factor in determining the categorized Hb abnormalities along with RBC indices. An HbA2 level of >3.9% was used as a cut-off for diagnosis of β-thalassemia trait (βTT), < 2.0% was used for α-thalassemia trait (αTT), and borderline values were fixed within the range of 3.6–3.9% [12].

Statistical analysis

The socio-demographic profile was summarized with numbers and percentages. Hematological indicators of CBC were presented as the mean and standard deviation. The prevalence of hemoglobinopathies was computed as a number and percentage. All analyses were performed using STATA version 17.0.

Results

Table 1 represents the socio-demographic profile of Malayali tribes in the Jawadhu hills of Tamil Nadu. A total of 650 tribes were enrolled and 443 blood samples were collected from them. Among the 443 participants, 234 (n = 52.82%) were males and 209 (n = 47.18%) were females. The majority of them (n = 46.50%) were in the age group of 6–15 years. Of the total participants, 25.73% (n = 114) were married; there was a practice of consanguinity in 71 or 62.28%, of the total marriages, while 52 or 45.61% of such consanguinity marriages took place within the same clan group. Of the total number of 443 participants, 10.61% (n = 47) only knew about hemoglobinopathies, 7.45% (n = 33) were illiterate or informal literate, 15.58% (n = 69) were unemployed or jobless, and 35.90% (n = 28) were earning less than ₹ 2,000 per month.

Table 1. Socio-demographic profile of Malayali tribes in the Jawadhu hills of Tamil Nadu.

Variable	n	%
Individual status
Willing to participate	443	68.15
Not willing to participate	207	31.85
Gender
Male	234	52.82
Female	209	47.18
Age
Less than 6 years	31	7.00
6 years to 15 years	206	46.50
16 years to 25 years	117	26.41
26 years to 35 years	89	20.09
Religion
Hindu	442	99.77
Muslim	1	0.23
Family type
Nuclear	431	97.29
Joint	5	1.13
Extended	7	1.58
Marital status
Married	114	25.73
Consanguinity marriage (n = 114)	71	62.28
Consanguinity marriage type (n = 71)
First cousin	5	7.04
Second cousin	8	11.27
Distant relative	58	81.69
Consanguinity marriage happened in family (n = 114)	52	45.61
Known about haemoglobinopathies	47	10.61
Education
Illiterate/Informal literate	33	7.45
School	348	78.55
Graduation/Diploma/Others	40	9.03
Not applicable	22	4.97
Occupation
Unemployed/Jobless	69	15.58
Employed/Business/Labor	78	17.60
Student	246	55.53
Not applicable	50	11.29
Income per month (₹)
Up to 2,000	28	35.90
2,001–5,000	15	19.23
5,001–10,000	22	28.20
Above 10,000	13	16.67

Table 2 shows the prevalence of various hemoglobinopathies among Malayali tribes in the Jawadhu hills of Tamil Nadu. Of the 443 tribal participants, 14.67% (n = 65) had an abnormal Hb fraction, whereas 83.30% (n = 369; Figure 2A) were identified as normal, and 2.03% (n = 9; Figure 2D) were borderline. The prevalence of αTT was 0.68% (n = 3; Figure 2B), while βTT was 13.99% (n = 62; Figure 2C).

Figure 2. Indicative chromatogram of different hemoglobinopathies (A). Normal, (B). α-thalassemia trait (C). β-thalassemia trait and (D). Borderline.

Table 2. Prevalence of various haemoglobinopathies among the Malayali tribes in the Jawadhu hills of Tamil Nadu.

Variable	n	%
Normal	369	83.30
α-thalassemia trait	3	0.68
β-thalassemia trait	62	13.99
Borderline	9	2.03
Total	443	100

Table 3 shows the RBC indices and hemoglobin fractions of Malayali tribes in the Jawadhu hills of Tamil Nadu. In the present study, hematocrit (HCT), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), and mean corpuscular hemoglobin concentration (MCHC) are very low in the αTT (30.13%, 63.60 fL, 20.50 pg and 31.87 g/dL) and βTT (36.57%, 67.68 fL, 22.50 pg and 33.24 g/dL) when compared to the normal (37.37%, 74.53 fL, 25.08 pg and 33.59 g/dL) participants. In addition, the HbA2 value was abnormal in αTT (1.77%) and βTT (5.92%) when compared to normal (2.92%).

Table 3. RBC indices and hemoglobin fractions of Malayali tribes in the Jawadhu hills of Tamil Nadu.

Hematological indices	Normal	α-thalassemia trait	β-thalassemia trait	Borderline
RBC (x10^6/µL)	5.04 ± 0.55	4.77 ± 0.29	5.43 ± 0.71	4.79 ± 0.19
WBC (x10^3/µL)	8.73 ± 2.28	8.75 ± 0.57	8.31 ± 2.3	8.08 ± 2.05
PLT (x10^3/µL)	287.31 ± 83.79	192.00 ± 142.28	272.27 ± 86.71	340.78 ± 80.48
HCT (%)	37.37 ± 4.33	30.13 ± 7.00	36.57 ± 5.27	37.31 ± 5.16
MCV (fL)	74.53 ± 8.34	63.60 ± 17.81	67.68 ± 7.39	78.09 ± 11.21
MCH (pg)	25.08 ± 3.29	20.50 ± 6.76	22.50 ± 2.61	26.27 ± 4.88
MCHC (g/dL)	33.59 ± 1.06	31.87 ± 1.91	33.24 ± 0.93	33.37 ± 2.23
RDW-CV (%)	14.77 ± 7.11	18.80 ± 5.27	15.58 ± 2.47	13.90 ± 2.60
RDW-SD (fL)	39.99 ± 4.98	42.33 ± 2.48	39.09 ± 5.79	40.24 ± 2.02
Hb (g/dL)	12.57 ± 1.66	9.70 ± 2.75	12.17 ± 1.84	12.52 ± 2.26
HbA0 (%)	87.42 ± 39.41	84.87 ± 1.20	82.59 ± 1.16	84.91 ± 1.12
HbA2 (%)	2.92 ± 0.32	1.77 ± 0.12	5.92 ± 0.72	3.69 ± 0.11
HbF (%)	1.48 ± 0.87	0.80 ± 0.06	1.15 ± 0.52	1.51 ± 0.85

Figure 3 shows the prevalence of anemia and its severity among the Malayali tribes in the Jawadhu hills of Tamil Nadu. Out of 234 male participants, 54.27% (n = 127) were normal, whereas 36.33% (n = 85) had mild anemia, 8.55% (n = 20) had moderate anemia, and 0.85% (n = 2) had severe anemia. Likewise, out of 209 female participants, 50.24% (n = 105) were normal, while 27.75% (n = 58) had mild anemia, 19.62% (n = 41) had moderate anemia, and 2.39% (n = 5) had severe anemia.

Figure 3. Prevalence of anemia and its severities among Malayali tribes in the Jawadhu hills of Tamil Nadu.

Discussion

Health is one of the prime concerns of human beings all over the world. In India, the health statuses of the tribal communities are very poor, which is dependent upon socio-demographic, economic, socio-cultural, dietary, and ecological factors [30,31]. Therefore, tribal people are unable to fulfill even their basic requirements, such as food, clothes, housing, and medicines. They are mainly neglected, exploited, and highly susceptible to diseases with an increased level of morbidity, mortality, and malnutrition [32,33], thus marginalized from the general community. In the present study, we have identified Malayali tribes residing in the Jawadhu hills as being affected socially, economically, and healthily. In the recent past, few studies reported the social, health, and economic status of Malayali tribes in Jawadhu hills, and their published results were also in line with the present study [34–36].

Every year, 10,000 children with β-thalassemia major are born in India, which comprises 10% of the total number in the world [37]. In contrast to the global frequency of 1.5%, the average carriers of βTT in India comprise 3.3% of the population [38]. In the Valsad district region of Gujarat, 0.25% of cases were βTT and 0.33% were β-thalassemia major reported in various tribal communities by Mistry et al. [39]. In Sundargarh district of north-western Orissa, the βTT was detected in an average of 6.5% of the Bhutyan tribe [40]. In Madhya Pradesh state, 1.4% of the βTT was reported in various tribes by Chourasia et al. [15]. In the Assam state, 3.07% of β-thalassemia prevalence was reported among the Munda ethnic tribes working in the tea gardens [41]. The present study, for the first time reported the prevalence of hemoglobinopathies in the Jawadhu Hills region, and the prevalence of βTT was 13.99%, αTT was 0.68%, and the borderline was 2.03%.

Anemia is a global public health problem, mainly affecting poor people in developing countries because their diet lacks specific vitamins and minerals [42]. It is a condition due to a reduction in the number of RBCs or a reduction in the concentration of blood Hb and/or HCT. This condition leads to insufficiency in oxygen-carrying capacity to meet the body's physiological needs [43,44]. In this study, around 45% to 50% of tribal participants were diagnosed with anemia, classified into mild, moderate, and severe categories. Saravanakumar et al. [45] reported that the prevalence of anemia was 76% in the Irular tribes of Jawadhu Hills, Tiruvannamalai district, which is higher than the present study.

Conclusion

‘Healthy people can create a healthy society and a healthier future for mankind.’ Health care is one of the most important of all human endeavors to improve the quality of life, especially for tribal people. Ethnic tribes are an important segment of society for their traditional life history and unique lifestyle. Their health and diseased conditions are also determining the future of the offspring. The tribal people have no clear concept of health and don't care about their health conditions. Even conceived women are not interested in having regular medical check-ups and taking modern medicines; instead, they follow their age-old traditions, customs, and practices. Hence, this needs special attention for creating general awareness among the masses and also to inculcate self-directed voluntariness and willingness to participate in the existing hemoglobinopathies screening programs within their village, block, taluk, or district level to utilize the public health care facilities for their well-being, as well as in insisting on the importance of their healthy living conditions supported by the government health systems and NGOs.

Author contributions

BG and SKA conceptualized the work; TR and BG performed the literature search. TR wrote the first draft of the manuscript. BG carried out the first draft revision. SD and VR performed the data analysis. SKA, AN, SR, and HK gave critical inputs. BG, TR, SKA, SD, VR, JY, AN, SR, and HK performed the review-editing of the manuscript and revisions. The decision of the final version is agreed upon by all the authors.

Acknowledgments

The authors acknowledged financial support from the Ministry of Health and Family Welfare, Government of India through the ICMR Extramural Research Grants, New Delhi. The authors would like to thank Mr. M. Venkatesan and Mr. Y. Isaac Arpudha Rangam (Project Senior Investigators), Ms. P. Pradeepa and Ms. A. Vinothini (Project Laboratory Technicians), Mr. V. Manoj Kumar (Project Data Entry Operator), Mr. P. Arun (Project Lab Attendant), Mr. G. Sundaramurthy and Mr. S. Vetrivel (Project Semi-Skilled Workers), Mrs. S. Dhana Priya Vadhani (Technician-2), and Mrs. V. M. Girija Lakshmi (Technical Officer-C) who were immensely involved in the field survey activities, data collection, biological sample collection, processing, and analysis. The authors are also grateful to Primary Health Centre (PHC) doctors and community leaders of the Malayali tribes for their kind support and cooperation.

We sincerely acknowledged our thanks and gratitude to our Head of the Institute ‘The Director, ICMR-National Institute of Epidemiology (ICMR-NIE), Chennai’ for his constant and consistent support and approval for overall field surveillance activities. Similarly, we also sincerely acknowledged our gratitude to ‘The Director, Directorate of Public Health & Preventive Medicine (DPH&PM), Government of Tamil Nadu’, ‘The Principal Chief Conservator of Forests (PCCF), and The District Forest Office (DFO), Government of Tamil Nadu’, ‘The Tribal Welfare Department (TWD), Government of Tamil Nadu’, and ‘The District Collectorate (DC), Tiruvannamalai District’ for their overall support and coordination in all our field public health survey activities. Finally, we extend our special thanks to all the study participants who consented and cooperated to participate in the study.

Disclosure statement

All the authors declared ‘No Conflicts of Interest’ in preparation of this original research manuscript, and publication of the study report.

Additional information

Funding

This study was funded by the ICMR Extramural Research grant with ICMR Extramural Research Grants No. Tribal/CFP/4/2018-ECD-II Dated 14/05/2019 [IRIS ID No. 2018-3075].