Prevalence of Glucose-6-Phosphate Dehydrogenase (G6PD) Deficiency among Malaria Patients in Southern Thailand: 8 Years Retrospective Study |
Khammanee, Thunchanok
(Division of Biological Science, Faculty of Science, Prince of Songkla University)
Sawangjaroen, Nongyao (Division of Biological Science, Faculty of Science, Prince of Songkla University) Buncherd, Hansuk (Faculty of Medical Technology, Prince of Songkla University) Tun, Aung Win (Faculty of Graduate Studies, Mahidol University) Thanapongpichat, Supinya (Faculty of Medical Technology, Prince of Songkla University) |
1 | Kaplan JC. Defective molecular variants of glucose-6-phosphate dehydrogenase and methaemoglobin reductase. J Clin Pathol Suppl (R Coll Pathol) 1974; 8: 134-141. DOI |
2 | Lo E, Zhong D, Raya B, Pestana K, Koepfli C, Lee MC, Yewhalaw D, Yan G. Prevalence and distribution of G6PD deficiency: implication for the use of primaquine in malaria treatment in Ethiopia. Malar J 2019; 18: 340. https://doi.org/10.1186/s12936-019-2981-x DOI |
3 | Ayi K, Turrini F, Piga A, Arese P. Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood 2004; 104: 3364-3371. https://doi.org/10.1182/blood-2003-11-3820 DOI |
4 | World Health Organization. Guide to G6PD Deficiency Rapid Diagnostic Testing to Support P. vivax Radical Cure. World Health Organization. Geneva, Switzerland. 2018. https://apps.who.int/iris/bitstream/handle/10665/272971/9789241514286-eng.pdf |
5 | Gomez-Manzo S, Terron-Hernandez J, De la Mora-De la Mora I, Gonzalez-Valdez A, Marcial-Quino J, Garcia-Torres I, VanoyeCarlo A, Lopez-Velazquez G, Hernandez-Alcantara G, OriaHernandez J, Reyes-Vivas H, Enriquez-Flores S. The stability of G6PD is affected by mutations with different clinical phenotypes. Int J Mol Sci 2014; 15: 21179-21201. https://doi.org/10.3390/ijms151121179 DOI |
6 | Au SW, Gover S, Lam VM, 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. https://doi.org/10.1016/s0969-2126(00)00104-0 DOI |
7 | Bancone G, Chu CS. G6PD Variants and haemolytic sensitivity to primaquine and other drugs. Front Pharmacol 2021; 12: 638885. https://doi.org/10.3389/fphar.2021.638885 DOI |
8 | Jiang W, Yu G, Liu P, Geng Q, Chen L, Lin Q, Ren X, Ye W, He Y, Guo Y, Duan S, Wen J, Li H, Qi Y, Jiang C, Zheng Y, Liu C, Si E, Zhang Q, Tian Q, Du C. Structure and function of glucose6-phosphate dehydrogenase-deficient variants in Chinese population. Hum Genet 2006; 119: 463-478. https://doi.org/10.1007/s00439-005-0126-5 DOI |
9 | 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 DOI |
10 | Lee J, Kim TI, Kang JM, Jun H, Le HG, Thai TL, Sohn WM, Myint MK, Lin K, Kim TS, Na BK. Prevalence of glucose-6-phosphate dehydrogenase (G6PD) deficiency among malaria patients in Upper Myanmar. BMC Infect Dis 2018; 18: 131. https://doi.org/10.1186/s12879-018-3031-y DOI |
11 | Boonyuen U, Songdej D, Tanyaratsrisakul S, Phuanukoonnon S, Chamchoy K, Praoparotai A, Pakparnich P, Sudsumrit S, Edwards T, Williams CT, Byrne RL, Adams ER, Imwong M. Glucose6-phosphate dehydrogenase mutations in malaria endemic area of Thailand by multiplexed high-resolution melting curve analysis. Malar J 2021; 20: 194. https://doi.org/10.1186/s12936-021-03731-0 DOI |
12 | Lopez C, Saravia C, Gomez A, Hoebeke J, Patarroyo MA. Mechanisms of genetically-based resistance to malaria. Gene 2010 467: 1-12. https://doi.org/10.1016/j.gene.2010.07.008 DOI |
13 | Udom C, Thanispong K, Manguin S, Chareonviriyaphap T, Fungfuang W. Trophic Behavior and species diversity of the Anopheles barbirostris Complex (Diptera: Culicidae) in Thailand. J Med Entomol 2021; 58: 2376-2384. https://doi.org/10.1093/jme/tjab067 DOI |
14 | Rueangweerayut R, Bancone G, Harrell EJ, Beelen AP, Kongpatanakul S, Mohrle JJ, Rousell V, Mohamed K, Qureshi A, Narayan S, Yubon N, Miller A, Nosten FH, Luzzatto L, Duparc S, Kleim JP, Green JA. Hemolytic potential of tafenoquine in female volunteers heterozygous for glucose-6-phosphate dehydrogenase (G6PD) deficiency (G6PD Mahidol Variant) versus G6PD-normal volunteers. Am J Trop Med Hyg 2017; 97: 702-711. https://doi.org/10.4269/ajtmh.16-0779 DOI |
15 | Chu CS, Bancone G, Nosten F, White NJ, Luzzatto L. Primaquineinduced haemolysis in females heterozygous for G6PD deficiency. Malar J 2018; 17: 101. https://doi.org/10.1186/s12936-018-2248-y DOI |
16 | Chu CS, Bancone G, Soe NL, Carrara VI, Gornsawun G, Nosten F. The impact of using primaquine without prior G6PD testing: a case series describing the obstacles to the medical management of haemolysis. Wellcome Open Res 2019; 4: 25. https://doi.org/10.12688/wellcomeopenres.15100.2 DOI |
17 | Frank JE. Diagnosis and management of G6PD deficiency. Am Fam Physician 2005; 72: 1277-1282. |
18 | Wang J, Luo E, Hirai M, Arai M, Abdul-Manan E, Mohamed-Isa Z, Hidayah N, Matsuoka H. Nine different glucose-6-phosphate dehydrogenase (G6PD) variants in a Malaysian population with Malay, Chinese, Indian and Orang Asli (aboriginal Malaysian) backgrounds. Acta Med Okayama 2008; 62: 327-332. https://doi.org/10.18926/AMO/30966 DOI |
19 | 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 DOI |
20 | Pathak V, Colah R, Ghosh K. Effect of inherited red cell defects on growth of Plasmodium falciparum: An in vitro study. Indian J Med Res 2018; 147: 102-109. https://doi.org/10.4103/ijmr.IJMR_1146_16 DOI |
21 | Cappadoro M, Giribaldi G, O'Brien E, Turrini F, Mannu F, Ulliers D, Simula G, Luzzatto L, Arese P. Early phagocytosis of glucose6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 1998; 92: 2527-2534. https://doi.org/10.1182/blood.V92.7.2527 DOI |
22 | Ninokata A, Kimura R, Samakkarn U, Settheetham-Ishida W, Ishida T. Coexistence of five G6PD variants indicates ethnic complexity of Phuket islanders, Southern Thailand. J Hum Genet 2006; 51: 424-428. https://doi.org/10.1007/s10038-006-0380-y DOI |
23 | Schoone GJ, Oskam L, Kroon NC, Schallig HD, Omar SA. Detection and quantification of Plasmodium falciparum in blood samples using quantitative nucleic acid sequence-based amplification. J Clin Microbiol 2000; 38: 4072-5407. https://doi.org/10.1128/JCM.38.11.4072-4075.2000 DOI |
24 | Iwagami M, Nakatsu M, Khattignavong P, Soundala P, Lorphachan L, Keomalaphet S, Xangsayalath P, Kawai S, Hongvanthong B, Brey PT, Kano S. First case of human infection with Plasmodium knowlesi in Laos. PLoS Negl Trop Dis 2018; 12: e0006244. https://doi.org/10.1371/journal.pntd.0006244 DOI |
25 | Uyoga S, Ndila CM, Macharia AW, Nyutu G, Shah S, Peshu N, Clarke GM, Kwiatkowski DP, Rockett KA, Williams TN. Glucose6-phosphate dehydrogenase deficiency and the risk of malaria and other diseases in children in Kenya: a case-control and a cohort study. Lancet Haematol 2015; 2: 437-444. https://doi.org/10.1016/S2352-3026(15)00152-0 DOI |
26 | Gomez-Manzo S, Marcial-Quino J, Ortega-Cuellar D, SerranoPosada H, Gonzalez-Valdez A, Vanoye-Carlo A, HernandezOchoa B, Sierra-Palacios E, Castillo-Villanueva A, Reyes-Vivas H. Functional and biochemical analysis of glucose-6-phosphate dehydrogenase (G6PD) variants: elucidating the molecular basis of G6PD deficiency. Catalysts 2017; 7: 135. https://doi.org/10.3390/catal7050135 DOI |
27 | Luzzatto L, Nannelli C, Notaro R. Glucose-6-phosphate dehydrogenase deficiency. Hematol Oncol Clin North Am 2016; 30: 373-393. https://doi.org/10.1016/j.hoc.2015.11.006 DOI |
28 | Piomelli S, Corash LM, Davenport DD, Miraglia J, Amorosi EL. In vivo lability of glucose-6-phosphate dehydrogenase in GdA-and GdMediterranean deficiency. J Clin Invest 1968; 47: 940-948. https://doi.org/10.1172/JCI105786 DOI |
29 | Khim N, Benedet C, Kim S, Kheng S, Siv S, Leang R, Lek S, Muth S, Chea N, Chuor CM, Duong S, Kerleguer A, Tor P, Chim P, Canier L, Witkowski B, Taylor WR, Menard D. G6PD deficiency in Plasmodium falciparum and Plasmodium vivax malaria-infected Cambodian patients. Malar J 2018; 12: 171. https://doi.org/10.1186/1475-2875-12-171 DOI |
30 | Cappellini MD, Fiorelli G. Glucose-6-phosphate dehydrogenase deficiency. Lancet 2008; 371: 64-74. https://doi.org/10.1016/S0140-6736(08)60073-2 DOI |
31 | Recht J, Ashley EA, White NJ. Use of primaquine and glucose6-phosphate dehydrogenase deficiency testing: divergent policies and practices in malaria endemic countries. PLoS Negl Trop Dis 2018; 12: e0006230. https://doi.org/10.1371/journal.pntd.0006230 DOI |
32 | Yusoff NM, Shirakawa T, Nishiyama K, Ghazali S, Ee CK, Orita A, Abdullah WZ, Isa MN, Van Rostenberghe H, Matsuo M. Molecular heterogeneity of glucose-6-phosphate dehydrogenase deficiency in Malays in Malaysia. Int J Hematol 2002; 76: 149-152. https://doi.org/10.1007/BF02982577 DOI |
33 | USAID. President's Malaria Initiative: Thailand, Lao PDR and Regional Abbreviated Malaria Operation Plan FY 2019 [Internet]. United States Agency for International Development; [cited 2022 Jan 22]. Available from: https://d1u4sg1s9ptc4z.cloudfront.net/uploads/2021/03/fy-2019-thailand-abbreviated-malaria-operational-plan.pdf |
34 | Jitueakul S, Buncherd H, Thawornpan P, Tun AW, Thanapongpichat S. Characterization of G6PD genotypes in G6PD deficiency patients from Suratthani Hospital, Thailand. JAMS 2018; 51: 66-71. |
35 | 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: 191-196. https://doi.org/10.1016/j.bcmd.2004.11.001 DOI |
36 | Bancone G, Chu CS, Somsakchaicharoen R, Chowwiwat N, Parker DM, Charunwatthana P, White NJ, Nosten FH. Characterization of G6PD genotypes and phenotypes on the northwestern Thailand-Myanmar border. PLoS One. 2014; 9: e116063. https://doi.org/10.1371/journal.pone.0116063 DOI |
37 | Price RN, von Seidlein L, Valecha N, Nosten F, Baird JK, White NJ. Global extent of chloroquine-resistant Plasmodium vivax: a systematic review and meta-analysis. Lancet Infect Dis 2014; 14: 982-991. https://doi.org/10.1016/S1473-3099(14)70855-2. DOI |
38 | Howes RE, Piel FB, Patil AP, Nyangiri OA, Gething PW, Dewi M, Hogg MM, Battle KE, Padilla CD, Baird JK, Hay SI. G6PD deficiency prevalence and estimates of affected populations in malaria endemic countries: a geostatistical model-based map. PLoS Med 2012; 9: e1001339. https://doi.org/10.1371/journal.pmed.1001339 DOI |
39 | Guindo A, Fairhurst RM, Doumbo OK, Wellems TE, Diallo DA. X-linked G6PD deficiency protects hemizygous males but not heterozygous females against severe malaria. PLoS Med 2007; 4: e66. https://doi.org/10.1371/journal.pmed.0040066 DOI |
40 | World Health Organization. Testing for G6PD deficiency for safe use of primaquine in radical cure of P. vivax and P. ovale: Policy brief. Geneva, Switzerland. World Health Organization. 2016. https://apps.who.int/iris/handle/10665/250297 |
41 | Nkhoma ET, Poole C, Vannappagari V, Hall SA, Beutler E. The global prevalence of glucose-6-phosphate dehydrogenase deficiency: a systematic review and meta-analysis. Blood Cells Mol Dis 2009; 42: 267-278. https://doi.org/10.1016/j.bcmd.2008.12.005 DOI |
42 | Charoenkwan P, Tantiprabha W, Sirichotiyakul S, Phusua A, Sanguansermsri T. Prevalence and molecular characterization of glucose-6-phosphate dehydrogenase deficiency in northern Thailand. Southeast Asian J Trop Med Public Health 2014; 45: 187-193. |
43 | Kanchanavithayakul A, Prasittisa K, Kiat-Amornrak P, Chanda M, Kittiwatanasarn P, Nuchprayoon I, Cheepsunthorn CL. Prevalence of glucose 6-phosphate dehydrogenase deficiency and genetic mutations among karen and lao populations in thailand. Southeast Asian J Trop Med Public Health 2017; 48: 1308-1317. |
44 | Sathupak S, Leecharoenkiat K, Kampuansai J. Prevalence and molecular characterization of glucose-6-phosphate dehydrogenase deficiency in the Lue ethnic group of northern Thailand. Sci Rep 2021; 11: 2956. https://doi.org/10.1038/s41598-021-82477-w DOI |
45 | Phompradit P, Kuesap J, Chaijaroenkul W, Rueangweerayut R, Hongkaew Y, Yamnuan R, Na-Bangchang K. Prevalence and distribution of glucose-6-phosphate dehydrogenase (G6PD) variants in Thai and Burmese populations in malaria endemic areas of Thailand. Malar J 2011; 10: 368. https://doi.org/10.1186/1475-2875-10-368 DOI |
46 | Khammanee T, Sawangjaroen N, Buncherd H, Tun AW, Thanapongpichat S. A LAMP-SNP assay detecting C580Y mutation in Pfkelch13 gene from clinically dried blood spot samples. Korean J Parasitol 2021; 59: 15-22. https://doi.org/10.3347/kjp.2021.59.1.15 DOI |
47 | Bonito B, Polrat Wilairatana P, Tangpukdee N, Muangnoicharoen S, Poovorawan K, Srivicha Krudsood S. Prevalence of glucose6-phosphate dehydrogenase deficiency among vivax malaria patients at the Hospital for Tropical Diseases, Thailand. Southeast Asian J Trop Med Public Health 2019; 50: 211-216. |
48 | Thanapongpichat S, Khammanee T, Sawangjaroen N, Buncherd H, Tun AW. Genetic diversity of Plasmodium vivax in clinical isolates from Southern Thailand using PvMSP1, PvMSP3 (PvMSP3alpha, PvMSP3beta) genes and eight microsatellite markers. Korean J Parasitol 2019; 57: 469-479. https://doi.org/10.3347/kjp.2019.57.5.469 DOI |
49 | Khammanee T, Sawangjaroen N, Buncherd H, Tun AW, Thanapongpichat S. Molecular surveillance of Pfkelch13 and Pfmdr1 mutations in Plasmodium falciparum isolates from Southern Thailand. Korean J Parasitol 2019; 57: 369-377. https://doi.org/10.3347/kjp.2019.57.4.369 DOI |
50 | World Health Organization. Updating the WHO G6PD classification of variants and the International Classification of Diseases, 11th Revision (ICD-11). Malaria Policy Committee Meeting. Background document for Session 7. 2019 October 2-4; Geneva, Switzerland. https://www.who.int/malaria/mpac/mpac-october2019-session7-updating-G6PD-classification.pdf |
51 | Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN. Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol 1993; 58: 283-292. https://doi.org/10.1016/0166-6851(93)90050-8 DOI |
52 | Ainoon O, Yu YH, Amir Muhriz AL, Boo NY, Cheong SK, Hamidah NH. Glucose-6-phosphate dehydrogenase (G6PD) variants in Malaysian Malays. Hum Mutat 2003; 21: 101. https://doi.org/10.1002/humu.9103 DOI |
53 | Huang Y, Choi MY, Au SW, Au DM, Lam VM, Engel PC. Purification and detailed study of two clinically different human glucose 6-phosphate dehydrogenase variants, G6PD(Plymouth) and G6PD(Mahidol): Evidence for defective protein folding as the basis of disease. Mol Genet Metab 2008; 93: 44-53. https://doi. org/10.1016/j.ymgme.2007.08.122 DOI |