Cited by 28Diabetes and associated disordersDiabetes Management and ResearchPancreatic function and diabetes

Clinical features, biochemistry and HLA-DRB1 status in children and adolescents with diabetes in Dhaka, Bangladesh

Open access
Zabeen, Bedowra, Govender, Denira, Hassan, Zahid, Noble, Janelle Annette, Lane, Julie A., Mack, Steven John, Atkinson, Mark Alvin, Azad, Kishwar +2 more·2019·Diabetes Research and Clinical Practice

Abstract

Aims Little information is published on diabetes in young people in Bangladesh. We aimed to investigate the demographic, clinical, and biochemical features, and HLA-DRB1 alleles in new cases of diabetes affecting Bangladeshi children and adolescents <22 years of age. Methods The study was conducted at Bangladesh Institute of Research and Rehabilitation of Diabetes, Endocrine and Metabolic Disorders (BIRDEM) in Dhaka. One hundred subjects aged <22 years at diagnosis were enrolled. Demographic characteristics, clinical information, biochemical parameters (blood glucose, HbA1c, C-peptide, and autoantibodies against glutamic acid decarboxylase 65 (GADA) and islet antigen-2 (IA-2A) were measured. High-resolution DNA genotyping was performed for HLA-DRB1. Results Eighty-four subjects were clinically diagnosed as type 1 diabetes (T1D), seven as type 2 diabetes (T2D), and nine as fibrocalculous pancreatic disease (FCPD). Of the 84 with T1D, 37 (44%) were males and 47 (56%) females, with median age at diagnosis 13 years (y) (range 1.6-21.7) and peak age at onset 12-15 years. 85% of subjects were assessed within one month of diagnosis and all within eleven months. For subjects diagnosed with T1D, mean C-peptide was 0.46 ± 0.22 nmol/L (1.40 ± 0.59 ng/mL), with 9 (10.7%) IA-2A positive, 22 (26%) GADA positive, and 5 (6%) positive for both autoantibodies. Analysis of HLA-DRB1 genotypes revealed locus-level T1D association (p = 6.0E-05); DRB1*04:01 appeared predisposing (p < 3.0E-06), and DRB1*14:01 appeared protective (p = 1.7E-02). Conclusions Atypical forms of T1D appear to be more common in young people in Bangladesh than in European populations. This will be helpful in guiding more specific assessment at onset and potentially, expanding treatment options.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.diabres.2019.107894

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • C-peptide measurements and other advanced diagnostics and phenotyping are being implemented in youth in less advantaged regions who have been newly diagnosed with diabetes mellitus.

    “However, this picture is changing with C-peptide measurements and other advanced diagnostics and phenotyping being implemented in youth in less advantaged regions who have been newly diagnosed with diabetes mellitus93–98.”

    From The epidemiology of type 1 diabetes mellitus in older adults (2025) · cites this paper as [97]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 40

  1. [1]Katsarou A, Gudbjornsdottir S, Rawshani A, Dabelea D, Bonifacio E, Anderson BJ, Type 1 diabetes mellitus. Nat Rev Dis Prim 2017; 3: 17016. doi: 10.1038/nrdp.2017.16. 28358037 · DOI · Paper page
  2. [2]Craig Prof. ME, Jefferies C, Dabelea D, Balde N, Seth A, Donaghue KC. Definition, epidemiology, and classification of diabetes in children and adolescents. Pediatr Diabetes 2014; 19: 7– 19. doi: 10.1111/pedi.12186. 25182305 · DOI
  3. [3]Unnikrishnan AG, Bhatia E, Bhatia V, Bhadada SK, Sahay RK, Kannan A, Type 1 diabetes versus type 2 diabetes with onset in persons younger than 20 years of age. Ann N Y Acad Sci 2008; 1150: 239– 44. doi: 10.1196/annals.1447.056. 19120303 · DOI
  4. [4]Balasubramanian K, Dabadghao P, Bhatia V, Colman PG, Gellert SA, Bharadwaj U, High frequency of type 1B (idiopathic) diabetes in North Indian children with recent-onset diabetes. Diabetes Care 2003; 26: 2697. 12941746
  5. [5]Amutha A, Datta M, Unnikrishnan IR, Anjana RM, Rema M, Narayan KMV, Clinical profile of diabetes in the young seen between 1992 and 2009 at a specialist diabetes centre in south India. Prim Care Diabetes 2011; 5: 223– 9. doi: 10.1016/j.pcd.2011.04.003. 21601548 · DOI · Paper page
  6. [6]Atun R, Davies JI, Gale EAM, Bärnighausen T, Beran D, Kengne AP, Diabetes in sub-Saharan Africa: from clinical care to health policy. Lancet Diabetes Endocrinol 2017; 5. doi: 10.1016/S2213-8587(17)30181-X. 28688818 · DOI
  7. [8]Zabeen B, Nahar J, Tayyeb S, Mohsin F, Nahar N, Azad K. Characteristics of children and adolescents at onset of type 2 diabetes in a Tertiary Hospital in Bangladesh. Indian J Endocrinol Metab 2016; 20: 638– 42. doi: 10.4103/2230-8210.190544. 27730073 PMC5040043 · DOI
  8. [9]Zabeen B, Khaled Z, Nahar J, Nabi N, Mohsin F, Akhter S, Cataract in children and adolescents with fibrocalculous pancreatic diabetes. Mymensingh Med J 2013; 22: 331– 5. 23715357
  9. [10]Zabeen B, Nahar J, Tayyeb S, Nahar N, Azad K, Donaghue K. Fibrocalculous pancreatic diabetes in Bangladeshi children and adolescents—a not so rare form of secondary diabetes. Int J Diabetes Dev Ctries 2018; 38: 153– 7. doi: 10.1007/s13410-017-0563-4. · DOI
  10. [11]Mohsin F, Leslie R, Hawa M, Biswas K, Zabeen B, Nahar N, Clinical Profile and Autoantibody Status in Younger Onset Diabetes in Bangladesh. Pediatr Diabetes 2007; 8: 42.17991132
  11. [12]Type Azad K. 1 diabetes: The Bangladesh perspective. Indian J Endocrinol Metab 2015; 19: S9– 11. doi: 10.4103/2230-8210.155344. 25941662 PMC4413401 · DOI
  12. [13]WHO/IDF. Definition and Diagnosis of Diabetes Mellitus and Intermediate Hyperglycemia Rep a WHO/IDF Consult WHO, Geneva 2006: 1– 46. doi: 10.1109/PCT.2007.4538487. · DOI
  13. [14]WHO Multicentre Growth Reference Study Group. WHO child growth standards: length/height-for-age, weight-for-age, weight-for-length, weight-forheight and body mass index-for-age: methods and development. WHO Child Growth Stand 2006: 1– 312. doi: 10.4067/S0370-41062009000400012. · DOI
  14. [15]de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ 2007; 85: 660– 7. 18026621 PMC2636412
  15. [16]Fawwad A, Govender D, Ahmedani MY, Basit A, Lane JA, Mack SJ, Clinical features, biochemistry and HLA-DRB1 status in youth-onset type 1 diabetes in Pakistan. Diabetes Res Clin Pract 2019; 149: 9– 17. doi: 10.1016/j.diabres.2019.01.023. 30710658 PMC6456725 · DOI · Paper page
  16. [17]Chen JJ, Hollenbach JA, Trachtenberg EA, Just JJ, Carrington M, Ronningen KS, Hardy-Weinberg testing for HLA class II (DRB1, DQA1, DQB1, and DPB1) loci in 26 human ethnic groups. Tissue Antigens 1999; 54: 533– 42. 10674966
  17. [18]Hollenbach JA, Mack SJ, Thomson G, Gourraud P- A. Analytical methods for disease association studies with immunogenetic data. Methods Mol Biol 2012; 882: 245– 66. doi: 10.1007/978-1-61779-842-9_14. 22665238 PMC4209949 · DOI
  18. [20]Pappas DJ, Marin W, Hollenbach JA, Mack SJ. Bridging ImmunoGenomic Data Analysis Workflow Gaps (BIGDAWG): An integrated case-control analysis pipeline. Hum Immunol 2016; 77: 283– 7. doi: 10.1016/j.humimm.2015.12.006. 26708359 PMC4828284 · DOI
  19. [21]Lancaster AK, Single RM, Solberg OD, Nelson MP, Thomson G. PyPop update--a software pipeline for large-scale multilocus population genomics. Tissue Antigens 2007; 69 Suppl 1: 192– 7. doi: 10.1111/j.1399-0039.2006.00769.x. 17445199 PMC4369784 · DOI
  20. [22]Guo SW, Thompson EA. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 1992; 48: 361– 72. 1637966
  21. [23]Chen JJ, Thomson G. The variance for the disequilibrium coefficient in the individual Hardy-Weinberg test. Biometrics 1999; 55: 1269– 72. 11315081
  22. [24]Ogle GD, Abdullah M, Mason D, Januszewski AS, Besançon S. Insulin storage in hot climates without refrigeration: temperature reduction efficacy of clay pots and other techniques. Diabet Med 2016; 33. doi: 10.1111/dme.13194. 27472257 · DOI
  23. [25]Redondo MJ, Steck AK, Pugliese A. Genetics of type 1 diabetes. Pediatr Diabetes 2018; 19: 346– 53. doi: 10.1111/pedi.12597. 29094512 PMC5918237 · DOI · Paper page
  24. [27]Brorsson C, Hansen NT, Bergholdt R, Brunak S, Pociot F. The type 1 diabetes - HLA susceptibility interactome - Identification of HLA genotype-specific disease genes for type 1 diabetes. PLoS One 2010; 5: e9576. doi: 10.1371/journal.pone.0009576. 20221424 PMC2832689 · DOI
  25. [28]Varney MD, Valdes AM, Carlson JA, Noble JA, Tait BD, Bonella P, HLA DPA1, DPB1 alleles and haplotypes contribute to the risk associated with type 1 diabetes: Analysis of the type 1 diabetes genetics consortium families. Diabetes 2010; 59: 2055– 62. doi: 10.2337/db09-0680. 20424227 PMC2911060 · DOI
  26. [29]Redondo MJ, Kawasaki E, Mulgrew CL, Noble JA, Erlich HA, Freed BM, DR- and DQ-associated protection from type 1A diabetes: Comparison of DRB1*1401 and DQA1*0102-DQB1*0602. J Clin Endocrinol Metab 2000; 85: 3793– 7. doi: 10.1210/jc.85.10.3793. 11061540 · DOI
  27. [31]Erlich H, Valdes AM, Noble J, Carlson JA, Varney M, Concannon P, HLA DR-DQ haplotypes and genotypes and type 1 diabetes risk: analysis of the type 1 diabetes genetics consortium families. Diabetes 2008; 57: 1084– 92. doi: 10.2337/db07-1331. 18252895 PMC4103420 · DOI · Paper page
  28. [32]IDF. Eighth edition 2017. 2017. doi: 10.1016/S0140-6736(16)31679-8. · DOI · Paper page
  29. [33]Kalra S, Kalra B, Sharma A. Prevalence of type 1 diabetes mellitus in Karnal district, Haryana state, India. Diabetol Metab Syndr 2010; 2: 14. doi: 10.1186/1758-5996-2-14. 20214794 PMC2844357 · DOI
  30. [34]Balsa A, Zabeen B, Ogle G, Tayyeb S, Azad K. Incidence estimate of type 1 Diabetes in Youth in Dhaka 2017: 2017. doi: 10.1530/endoabs.49.EP428. · DOI
  31. [36]Usher-Smith JA, Thompson M, Ercole A, Walter FM. Variation between countries in the frequency of diabetic ketoacidosis at first presentation of type 1 diabetes in children: A systematic review. Diabetologia 2012; 55: 2878– 94. doi: 10.1007/s00125-012-2690-2. 22933123 PMC3464389 · DOI
  32. [37]Unnikrishnan R, Mohan V. Fibrocalculous pancreatic diabetes (FCPD). Acta Diabetol 2015; 52: 1– 9. doi: 10.1007/s00592-014-0685-9. 25395047 · DOI
  33. [38]Singh AK, Bhatia E, Dabadghao P, Bhatia V, Gellert SA, Colman PG. Role of islet autoimmunity in the aetiology of different clinical subtypes of diabetes mellitus in young north Indians. Diabet Med 2000; 17: 275– 80. 10821293
  34. [39]Biswas T, Islam A, Rawal LB, Islam SMS. Increasing prevalence of diabetes in Bangladesh: a scoping review. Public Health 2016; 138: 4– 11. doi: 10.1016/j.puhe.2016.03.025. 27169347 · DOI
  35. [40]Goswami R, Kochupillai N, Gupta N, Kukreja A, Lan M, Maclaren NK. Islet cell autoimmunity in youth onset diabetes mellitus in Northern India. Diabetes Res Clin Pract 2001; 53: 47– 54. 11378213
  36. [41]Tandon N, Shtauvere-Brameus A, Hagopian WA, Sanjeevi CB. Prevalence of ICA-12 and other autoantibodies in north Indian patients with early-onset diabetes. Ann N Y Acad Sci 2002; 958: 214– 7. 12021109
  37. [42]Dayal D, Samprati M, Kaur N, Ranjana WM, Jayaraman D. Prevalence of Beta-Cell, Thyroid and Celiac Autoimmunity in North Indian Children with Recent Onset Type 1 Diabetes (T1D). J Clin Diagnostic Res 2015; 9: 1– 2. doi: 10.1111/pedi.12200. PMC4413128 25954678 · DOI
  38. [43]Dabelea D, Pihoker C, Talton JW, D’Agostino RB, Fujimoto W, Klingensmith GJ, Etiological approach to characterization of diabetes type: The SEARCH for diabetes in youth study. Diabetes Care 2011; 34: 1628– 33. doi: 10.2337/dc10-2324. 21636800 PMC3120176 · DOI
  39. [44]Noble JA, Johnson J, Lane JA, Valdes AM. HLA class II genotyping of African American type 1 diabetic patients reveals associations unique to African haplotypes. Diabetes 2013. doi: 10.2337/db13-0094. PMC3749336 23801574 · DOI
  40. [45]Shivaprasad C, Mittal R, Dharmalingam M, Kumar PK. Zinc transporter-8 autoantibodies can replace IA-2 autoantibodies as a serological marker for juvenile onset type 1 diabetes in India. Indian J Endocrinol Metab 2014; 18: 345– 9. doi: 10.4103/2230-8210.131174. 24944929 PMC4056133 · DOI

Cited by

Sorted by citations

Authors
Zabeen, B., Govender, D., Hassan, Z., Noble, J. A., Lane, J. A., Mack, S. J., Atkinson, M. A., Azad, K., Wasserfall, C. H., & Ogle, G. D.
Affiliations
  • Bangladesh Institute of Research and Rehabilitation for Diabetes Endocrine and Metabolic Disorders (BD)
  • The University of Sydney (AU)
  • Bangladesh University of Health Sciences (BD)
  • University of Florida Health (US)
  • University of Florida (US)
Corresponding author
  • Govender, Denira
  • Hassan, Zahid
  • Noble, Janelle Annette
  • Lane, Julie A.
  • Mack, Steven John
  • Atkinson, Mark Alvin
  • Azad, Kishwar
  • Wasserfall, Clive Henry
  • Ogle, Graham David
Venue
Diabetes Research and Clinical Practice
Publisher
Elsevier BV
Published
2019-12
Volume
158
Pages
107894
ISSN
0168-8227 (ISSN-L)
OpenAlex
W2981837178
Cited by
28
References
3
Citations by year
2026: 3 · 2025: 2 · 2024: 7 · 2023: 4 · 2022: 6 · 2021: 3 · 2020: 3
FWCI
1.81
Type
journal article
Language
en
Open access
Locations
  • Diabetes Research and Clinical Practice (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
Leona M. and Harry B. Helmsley Charitable Trust
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
  • Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
  • Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
Keywords
type 1 diabetes, type 2 diabetes, HLA-DRB1, HLA-DRB1*0401, autoantibodies, GADA, IA-2A, C-peptide, HbA1c, children and adolescents, Bangladesh, age of onset, genetic susceptibility
MeSH terms
Adolescent, Adult, Bangladesh, C-Peptide, Child, Child, Preschool, Diabetes Mellitus, Type 2, Female, Humans, Infant, Male, Young Adult, HLA-DRB1 Chains

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review