PREVALENCE AND MOLECULAR CHARACTERIZATION OF GLUCOSE-6-PHOSPHATE DEHYDROGENASE (G6PD) DEFICIENCY IN FEMALES FROM PREVIOUSLY MALARIA ENDEMIC REGIONS IN NORTHEASTERN THAILAND AND IDENTIFICATION OF A NOVEL G6PD VARIANT
Main Article Content
Keywords
G6PD deficiency, Female, Northeastern Thailand, Novel G6PD variant
Abstract
Introduction: Glucose-6-phosphate dehydrogenase (G6PD) deficiency is the most common X-linked enzymopathy, highly prevalent in areas where malaria is or has been endemic. Prevalence of G6PD deficiency and characterization of G6PD variants in females from previously malaria endemic areas of northeast Thailand remain unstudied.
Methods: Prevalence of G6PD deficiency was determined by a fluorescent spot test (FST) and multiplex allele specific (AS)- and restriction fragment length polymorphic (RFLP)-PCR developed for detection of common G6PD variants in the Thai population.
Results: Prevalence of G6PD deficiency in female samples (n = 355) was 18% by FST and 27% by PCR-based genotyping. The most common variant was G6PD Viangchan (54%), followed by G6PD Canton (11%) and G6PD Union (11%); in addition, a novel heterozygous variant, G6PD Khon Kaen (c.305T>C, p.F102S located in the coenzyme-binding domain), was identified. The majority (75%) of G6PD activities of heterozygotes were within the intermediate deficiency range (30-80% of median normal enzyme activity).
Conclusion: High prevalence of G6PD deficiency was present in females from northeast Thailand, the majority being due to heterozygosity of G6PD variants. The findings will have a bearing on an inclusion of primaquine in antimalarial-based policies for malaria elimination in populations with high prevalence in G6PD deficiency.
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References
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PMid:14175196
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https://doi.org/10.1007/BF01474765
PMid:5715190
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https://doi.org/10.1186/s12889-020-8248-1
PMid:31992253 PMCid:PMC6986100
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https://doi.org/10.1111/j.1365-2141.1979.tb03774.x
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https://doi.org/10.1016/j.cca.2015.01.017
PMid:25632835
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https://doi.org/10.1016/j.ijbiomac.2017.06.002
PMid:28583873 PMCid:PMC5625996
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https://doi.org/10.1007/s10038-005-0279-z
PMid:16136268
32. Bancone G, Menard D, Khim N, Kim S, Canier L, Nguong C, Phommasone K, Mayxay M, Dittrich S, Vongsouvath M, Fievet N, Le Hesran JY, Briand V, Keomany S, Newton PN, Gorsawun G, Tardy K, Chu CS, Rattanapalroj O, Dong LT, Quang HH, Tam-Uyen N, Thuy-Nhien N, Hien TT, Kalnoky M, Nosten F. Molecular characterization and mapping of glucose-6-phosphate dehydrogenase (G6PD) mutations in the Greater Mekong Subregion. Malar J. 2019;18:20.
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https://doi.org/10.1016/j.bcmd.2004.11.001
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10.1016/s0969-2126(00)00104-0
PMid:10745013
https://doi.org/10.1016/j.bcmd.2008.12.005
PMid:29786478
2. Luzzatto L, Ally M, Notaro R. Glucose-6-phosphate dehydrogenase deficiency. Blood. 2020;136(11):1225-1240.
https://doi.org/10.1182/blood.2019000944
PMid:32764983 PMCid:PMC7371606
3. WHO Working Group. Glucose-6-phosphate dehydrogenase deficiency. Bull World Health Organ. 1989;67(6):601-611.
https://apps.who.int/iris/handle/10665/264721
PMid:2633878 PMCid:PMC2491315
4. World Health Organization. Guide to G6PD deficiency rapid diagnostic testing to support P. vivax radical cure. GenevaWorld Heal Organ. 2018. https://www.who.int/publications/i/item/9789241514286
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https://doi.org/10.5694/mja2.50474
PMid:32036613 PMCid:PMC7064913
6. Minucci A, Giardina B, Zuppi C, Capoluongo E. Glucose-6-phosphate dehydrogenase laboratory assay: how, when, and why? IUBMB Life. 2009;61(1):27-34.
https://doi.org/10.1002/iub.137
PMid:18942156
7. Pfeffer DA, Ley B, Howes RE, Adu P, Alam MS, Bansil P, Boum 2nd Y, Brito M, Charoenkwan P, Clements A, Cui L, Deng Z, Egesie OJ , Espino FE, Fricken ME, Hamid MMA, He Y, Henriques G, Khan WA, Khim N, Kim S, Lacerda M, Lon C, Mekuria AH, Menard D, Monteiro W, Nosten F, Oo NN, Pal S, Palasuwan D, Parikh S, Pasaribu AP, Poespoprodjo JR, Price DJ, Roca-Feltrer A, Roh ME, Saunders DL, Spring MD, Sutanto I, Thriemer K, Weppelmann TA, Seidlein L, Satyagraha AW, Bancone G, Domingo GJ, Price RN. Quantification of glucose-6-phosphate dehydrogenase activity by spectrophotometry: a systematic review and meta-analysis. PLoS Med. 2020;17(5).
https://doi.org/10.1371/journal.pmed.1003084
PMid:32407380 PMCid:PMC7224463
8. Kaplan M, Beutler E, Vreman HJ, Hammerman C, Levy-Lahad E, Renbaum P, Stevenson DK. Neonatal hyperbilirubinemia in glucose-6-phosphate dehydrogenase- deficient heterozygotes. Pediatrics. 1999;104:68-74.
https://doi.org/10.1542/peds.104.1.68
PMid:10390262
9. Zangen S, Kidron D, Gelbart T, Roy-Chowdhury N, Wang X, Kaplan M. Fatal kernicterus in a girl deficient in glucose-6-phosphate dehydrogenase: a paradigm of synergistic heterozygosity. J Pediatr. 2009;154(4):616-619.
https://doi.org/10.1016/j.jpeds.2008.10.049
PMid:19324225
10. Chu CS, Bancone G, Nosten F, White NJ, Luzzatto L. Primaquine-induced haemolysis in females heterozygous for G6PD deficiency. Malar J. 2018;17(1):101. https://doi.org/10.1186/s12936-018-2248-y
PMid:29499733 PMCid:PMC5833093
11. Chu CS, Freedman DO. Tafenoquine and G6PD: a primer for clinicians. J Travel Med. 2018;26(4):1-11.
https://doi.org/10.1093/jtm/taz023
PMid:30941413 PMCid:PMC6542331
12. Watson J, Rj Taylor W, Menard D, Kheng S, White NJ. Modelling primaquine-induced haemolysis in G6PD deficiency. Elife. 2017;6:e23061. https://doi.org/10.7554/eLife.23061
PMid:28155819 PMCid:PMC5330681
13. Petney T, Sithithaworn P, Satrawaha R, Warr CG, Andrews R, Wang YC, Feng CC. Potential malaria reemergence, northeastern Thailand. Emerg Infect Dis. 2009;15(8):1330-1331.
https://doi.org/10.3201/eid1508.090240
PMid:9751612 PMCid:PMC2815977
14. Imwong M, Dhorda M, Myo Tun K, Thu AM, Phyo AP, Proux S, Suwannasin K, Kunasol C, Srisutham S, Duanguppama J, Vongpromek R, Promnarate C, Saejeng A, Khantikul N, Sugaram R, Thanapongpichat S, Sawangjaroen N, Sutawong K, Han KT, Htut Y, Linn K, Win AA, Hlaing TM, van der Pluijm RW, Mayxay M, Pongvongsa T, Phommasone K, Tripura R, Peto TJ, von Seidlein L, Nguon C, Lek D, Chan XHS, Rekol H, Leang R, Huch C, Kwiatkowski DP, Miotto O, Ashley EA, Kyaw MP, Pukrittayakamee S, Day NPJ, Dondorp AM, Smithuis FM, Nosten FH, White NJ. Molecular epidemiology of resistance to antimalarial drugs in the Greater Mekong subregion: an observational study. Lancet Infect Dis. 2020.
https://doi.org/10.1016/S1473-3099(20)30228-0
PMid:32679084
15. Geng J, Malla P, Zhang J, Xu S, Li C, Zhao Y, Wang Q, Kyaw MP, Cao Y, Yang Z, Cui L. Increasing trends of malaria in a border area of the Greater Mekong Subregion. Malar J. 2019;18:309.
https://doi.org/10.1186/s12936-019-2924-6
PMid:31514740 PMCid:PMC6739967
16. Wasi P, Na-Nakorn S, Suingdumrong A. Studies of the distribution of haemoglobin E, thalassaemias and glucose-6-phosphate dehydrogenase deficiency in North-eastern Thailand. Nature. 1967;214(5087):501-502.
https://doi.org/10.1038/214501a0
PMid:6032880
17. Kruatrachue M, Charoenlarp P, Chongsuphajaisiddhi T, Harinasuta C. Erythrocyte glucose-6-phosphate dehydrogenase and malaria in Thailand. Lancet. 1962;2(7267):1183-1186.
https://doi.org/10.1016/s0140-6736(62)90956-x
PMid:13927068
18. Flatz G, Sringam S. Malaria and glucose-6-phosphate dehydrogenase deficiency in Thailand. Lancet. 1963;282(7320):1248-1250.
https://doi.org/10.1016/s0140-6736(63)90895-x
PMid:14066844
19. Flatz G, Sringam S. Glucose-6-phosphate dehydrogenase deficiency in different ethnic groups in Thailand. Ann Hum Genet. 1964;27:315-318.
https://doi.org/10.1111/j.1469-1809.1963.tb01528.x
PMid:14175196
20. Tuchinda S, Rucknagel DL, Na-Nakorn S, Wasi P. The Thai variant and the distribution of alleles of 6-phosphogluconate dehydrogenase and the distribution of glucose 6-phosphate dehydrogenase deficiency in Thailand. Biochem Genet. 1968;2(3):253-264.
https://doi.org/10.1007/BF01474765
PMid:5715190
21. Kittiwatanasarn P, Louicharoen C, Sukkapan P, Nuchprayoon I. Glucose-6-phosphate dehydrogenase deficiency in Northeastern Thailand: prevalence and relationship to neonatal jaundice. Chula Med J. 2003;47(8):471-479.
22. Jamnok J, Sanchaisuriya K, Sanchaisuriya P, Fucharoen G, Fucharoen S, Ahmed F. Factors associated with anaemia and iron deficiency among women of reproductive age in Northeast Thailand: a cross-sectional study. BMC Public Health. 2020;20:102.
https://doi.org/10.1186/s12889-020-8248-1
PMid:31992253 PMCid:PMC6986100
23. Beutler E, Blume KG, Kaplan JC, Löhr GW, Ramot B, Valentine WN. International Committee for Standardization in Haematology: recommended screening test for glucose-6-phosphate dehydrogenase (G-6-PD) deficiency. Br J Haematol. 1979;43(3):465-467.
https://doi.org/10.1111/j.1365-2141.1979.tb03774.x
PMid:497122
24. Kitcharoen S, Dechyotin S, Khemtonglang N, Kleesuk C. Relationship among glucose-6-phosphate dehydrogenase (G-6-PD) activity, G-6-PD variants and reticulocytosis in neonates of northeast Thailand. Clin Chim Acta. 2015;442:125-129.
https://doi.org/10.1016/j.cca.2015.01.017
PMid:25632835
25. Dallol A, Banni H, Gari MA, Al-Qahtani MH, Abuzenadeh AM, Al-Sayes F, Chaudhary AG, Bidwell J, Kafienah W. Five novel glucose-6-phosphate dehydrogenase deficiency haplotypes correlating with disease severity. J Transl Med. 2012;10:199.
https://doi.org/10.1186/1479-5876-10-199
PMid:23006493 PMCid:PMC3492101
26. Venselaar H, te Beek TAH, Kuipers RKP, Hekkelman ML, Vriend G. Protein structure analysis of mutations causing inheritable diseases. An e-Science approach with life scientist friendly interfaces. BMC Bioinformatics. 2010;11:548.
https://doi.org/10.1186/1471-2105-11-548
PMid:21059217 PMCid:PMC2992548
27. Poolsuwan S. Testing the “Malaria Hypothesis”for the Case of Thailand: A Genetic Appraisal. Hum Biol. 2003;75(4):585-605.
https://doi.org/10.1353/hub.2003.0061
PMid:14655879
28. Howes RE, Dewi M, Piel FB, Monteiro WM, Battle KE, Messina JP, Sakuntabhai A, Satyagraha AW, Williams TN, Baird JK, Hay SI. Spatial distribution of G6PD deficiency variants across malaria-endemic regions. Malar J. 2013;12:418.
https://doi.org/10.1186/1475-2875-12-418
PMid:24228846 PMCid:PMC3835423
29. Chu CS, Bancone G, Kelley M, Advani N, Domingo GJ, Cutiongo-de la Paz EM, van der Merwe N, Cohen J, Gerth-Guyette E. Optimizing G6PD testing for Plasmodium vivax case management and beyond: why sex, counseling, and community engagement matter. Wellcome Open Res. 2020;5:21.
https://doi.org/10.12688/wellcomeopenres.15700.2
PMid:32766454 PMCid:PMC7388194
30. Boonyuen U, Chamchoy K, Swangsri T, Junkree T, Day NPJ, White NJ, Imwong M. A trade off between catalytic activity and protein stability determines the clinical manifestations of glucose-6-phosphate dehydrogenase (G6PD) deficiency. Int J Biol Macromol. 2017;104:145-156.
https://doi.org/10.1016/j.ijbiomac.2017.06.002
PMid:28583873 PMCid:PMC5625996
31. Matsuoka H, Nguon C, Kanbe T, Jalloh A, Sato H, Yoshida S, Hirai M, Arai M, Socheat D, Kawamoto F. Glucose-6-phosphate dehydrogenase (G6PD) mutations in Cambodia: G6PD Viangchan (871G>A) is the most common variant in the Cambodian population. J Hum Genet. 2005;50(9):468-472.
https://doi.org/10.1007/s10038-005-0279-z
PMid:16136268
32. Bancone G, Menard D, Khim N, Kim S, Canier L, Nguong C, Phommasone K, Mayxay M, Dittrich S, Vongsouvath M, Fievet N, Le Hesran JY, Briand V, Keomany S, Newton PN, Gorsawun G, Tardy K, Chu CS, Rattanapalroj O, Dong LT, Quang HH, Tam-Uyen N, Thuy-Nhien N, Hien TT, Kalnoky M, Nosten F. Molecular characterization and mapping of glucose-6-phosphate dehydrogenase (G6PD) mutations in the Greater Mekong Subregion. Malar J. 2019;18:20.
https://doi.org/10.1186/s12936-019-2652-y
PMid:30674319 PMCid:PMC6343352
33. Laosombat V, Sattayasevana B, Janejindamai W, Viprakasit V, Shirakawa T, Nishiyama K, Matsuo M. Molecular heterogeneity of glucose-6-phosphate dehydrogenase (G6PD) variants in the south of Thailand and identification of a novel variant (G6PD Songklanagarind). Blood Cells Mol Dis. 2005;34(2):191-196.
https://doi.org/10.1016/j.bcmd.2004.11.001
PMid:15727905
34. Au SWN, Gover S, Lam VMS, Adams MJ. Human glucose-6-phosphate dehydrogenase: The crystal structure reveals a structural NADP+ molecule and provides insights into enzyme deficiency. Structure. 2000;8:293-303.
10.1016/s0969-2126(00)00104-0
PMid:10745013
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Apr 30, 2021
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Dechyotin, S. (2021) “PREVALENCE AND MOLECULAR CHARACTERIZATION OF GLUCOSE-6-PHOSPHATE DEHYDROGENASE (G6PD) DEFICIENCY IN FEMALES FROM PREVIOUSLY MALARIA ENDEMIC REGIONS IN NORTHEASTERN THAILAND AND IDENTIFICATION OF A NOVEL G6PD VARIANT”, Mediterranean Journal of Hematology and Infectious Diseases, 13(1), p. Page e2021029. doi: 10.4084/MJHID.2021.029.
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