Quantification of glucose-6-phosphate dehydrogenase activity by spectrophotometry: A systematic review and meta-analysis
Autoři:
Daniel A. Pfeffer aff001; Benedikt Ley aff001; Rosalind E. Howes aff002; Patrick Adu aff004; Mohammad Shafiul Alam aff005; Pooja Bansil aff006; Yap Boum, II aff007; Marcelo Brito aff009; Pimlak Charoenkwan aff010; Archie Clements aff011; Liwang Cui aff013; Zeshuai Deng aff014; Ochaka Julie Egesie aff015; Fe Esperanza Espino aff016; Michael E. von Fricken aff017; Muzamil Mahdi Abdel Hamid aff018; Yongshu He aff014; Gisela Henriques aff019; Wasif Ali Khan aff005; Nimol Khim aff020; Saorin Kim aff020; Marcus Lacerda aff009; Chanthap Lon aff021; Asrat Hailu Mekuria aff022; Didier Menard aff023; Wuelton Monteiro aff009; Francois Nosten aff024; Nwe Nwe Oo aff026; Sampa Pal aff006; Duangdao Palasuwan aff027; Sunil Parikh aff028; Ayodhia Pitaloka Pasaribu aff029; Jeanne Rini Poespoprodjo aff030; David J. Price aff031; Arantxa Roca-Feltrer aff033; Michelle E. Roh aff034; David L. Saunders aff021; Michele D. Spring aff021; Inge Sutanto aff037; Kamala Ley-Thriemer aff001; Thomas A. Weppelmann aff038; Lorenz von Seidlein aff024; Ari Winasti Satyagraha aff040; Germana Bancone aff024; Gonzalo J. Domingo aff006; Ric N. Price aff001
Působiště autorů:
Global and Tropical Health Division, Menzies School of Health Research and Charles Darwin University, Darwin, Australia
aff001; Malaria Atlas Project, Big Data Institute, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
aff002; Foundation for Innovative New Diagnostics, Geneva, Switzerland
aff003; Department of Medical Laboratory Sciences, School of Allied Health Sciences, University of Cape Coast, Cape Coast, Ghana
aff004; Infectious Diseases Division, International Centre for Diarrheal Diseases Research, Bangladesh, Mohakhali, Dhaka, Bangladesh
aff005; Diagnostics Program, PATH, Seattle, Washington, United States of America
aff006; Médecins sans Frontières Epicentre, Mbarara Research Centre, Mbarara, Uganda
aff007; Mbarara University of Science and Technology, Mbarara, Uganda
aff008; Fundação de Medicina Tropical Dr. Heitor Vieira Dourado, Manaus, Amazonas, Brasil
aff009; Division of Hematology and Oncology, Department of Pediatrics, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand
aff010; Faculty of Health Sciences, Curtin University, Bentley, Australia
aff011; Telethon Kids Institute, Nedlands, Australia
aff012; Department of Entomology, Pennsylvania State University, University Park, Pennsylvania, United States of America
aff013; Department of Cell Biology and Medical Genetics, Kunming Medical University, Kunming, Yunnan Province, China
aff014; Department of Hematology and Blood Transfusion, Faculty of Medical Sciences, University of Jos and Jos University Teaching Hospital, Jos, Plateau State, Nigeria
aff015; Department of Parasitology, Research Institute for Tropical Medicine, Department of Health, Alabang, Muntinlupa City, Philippines
aff016; Department of Global and Community Health, George Mason University, Fairfax, Virginia, United States of America
aff017; Department of Parasitology and Medical Entomology, Institute of Endemic Diseases, University of Khartoum, Khartoum, Republic of the Sudan
aff018; Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom
aff019; Malaria Molecular Epidemiology Unit, Institut Pasteur du Cambodge, Phnom Penh, Cambodia
aff020; Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand
aff021; School of Medicine, Addis Ababa University, Addis Ababa, Ethiopia
aff022; Malaria Genetics and Resistance Group, Institut Pasteur, Paris, France
aff023; Shoklo Malaria Research Unit, Mahidol–Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, Thailand
aff024; Centre for Tropical Medicine & Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
aff025; Department of Medical Research, Lower Myanmar, Yangon, Myanmar
aff026; Oxidation in Red Cell Disorders and Health Research Unit, Department of Clinical Microscopy, Faculty of Allied Health Sciences, Chulalongkorn University, Bangkok, Thailand
aff027; Yale School of Public Health, New Haven, Connecticut, United States of America
aff028; Faculty of Medicine, Universitas Sumatera Utara, Medan, Indonesia
aff029; Yayasan Pengembangan Kesehatan dan Masyarakat Papua (YPKMP), Papua, Indonesia
aff030; Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Australia
aff031; The Peter Doherty Institute for Infection and Immunity, The University of Melbourne and Royal Melbourne Hospital, Melbourne, Australia
aff032; Malaria Consortium, Phnom Penh, Cambodia
aff033; Global Health Group, Malaria Elimination Initiative, University of California, San Francisco, San Francisco, United States of America
aff034; F. Edward Hebert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda, Maryland, United States of America
aff035; US Army Medical Materiel Development Activity, Fort Detrick, Maryland, United States of America
aff036; University of Indonesia, Jakarta, Indonesia
aff037; Herbert Wertheim College of Medicine, Florida International University, Miami, Florida, United States of America
aff038; Mahidol Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
aff039; Eijkman Institute for Molecular Biology, Jakarta, Indonesia
aff040
Vyšlo v časopise:
Quantification of glucose-6-phosphate dehydrogenase activity by spectrophotometry: A systematic review and meta-analysis. PLoS Med 17(5): e32767. doi:10.1371/journal.pmed.1003084
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pmed.1003084
Souhrn
Background
The radical cure of Plasmodium vivax and P. ovale requires treatment with primaquine or tafenoquine to clear dormant liver stages. Either drug can induce haemolysis in individuals with glucose-6-phosphate dehydrogenase (G6PD) deficiency, necessitating screening. The reference diagnostic method for G6PD activity is ultraviolet (UV) spectrophotometry; however, a universal G6PD activity threshold above which these drugs can be safely administered is not yet defined. Our study aimed to quantify assay-based variation in G6PD spectrophotometry and to explore the diagnostic implications of applying a universal threshold.
Methods and findings
Individual-level data were pooled from studies that used G6PD spectrophotometry. Studies were identified via PubMed search (25 April 2018) and unpublished contributions from contacted authors (PROSPERO: CRD42019121414). Studies were excluded if they assessed only individuals with known haematological conditions, were family studies, or had insufficient details. Studies of malaria patients were included but analysed separately. Included studies were assessed for risk of bias using an adapted form of the Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2) tool. Repeatability and intra- and interlaboratory variability in G6PD activity measurements were compared between studies and pooled across the dataset. A universal threshold for G6PD deficiency was derived, and its diagnostic performance was compared to site-specific thresholds. Study participants (n = 15,811) were aged between 0 and 86 years, and 44.4% (7,083) were women. Median (range) activity of G6PD normal (G6PDn) control samples was 10.0 U/g Hb (6.3–14.0) for the Trinity assay and 8.3 U/g Hb (6.8–15.6) for the Randox assay. G6PD activity distributions varied significantly between studies. For the 13 studies that used the Trinity assay, the adjusted male median (AMM; a standardised metric of 100% G6PD activity) varied from 5.7 to 12.6 U/g Hb (p < 0.001). Assay precision varied between laboratories, as assessed by variance in control measurements (from 0.1 to 1.5 U/g Hb; p < 0.001) and study-wise mean coefficient of variation (CV) of replicate measures (from 1.6% to 14.9%; p < 0.001). A universal threshold of 100% G6PD activity was defined as 9.4 U/g Hb, yielding diagnostic thresholds of 6.6 U/g Hb (70% activity) and 2.8 U/g Hb (30% activity). These thresholds diagnosed individuals with less than 30% G6PD activity with study-wise sensitivity from 89% (95% CI: 81%–94%) to 100% (95% CI: 96%–100%) and specificity from 96% (95% CI: 89%–99%) to 100% (100%–100%). However, when considering intermediate deficiency (<70% G6PD activity), sensitivity fell to a minimum of 64% (95% CI: 52%–75%) and specificity to 35% (95% CI: 24%–46%). Our ability to identify underlying factors associated with study-level heterogeneity was limited by the lack of availability of covariate data and diverse study contexts and methodologies.
Conclusions
Our findings indicate that there is substantial variation in G6PD measurements by spectrophotometry between sites. This is likely due to variability in laboratory methods, with possible contribution of unmeasured population factors. While an assay-specific, universal quantitative threshold offers robust diagnosis at the 30% level, inter-study variability impedes performance of universal thresholds at the 70% level. Caution is advised in comparing findings based on absolute G6PD activity measurements across studies. Novel handheld quantitative G6PD diagnostics may allow greater standardisation in the future.
Klíčová slova:
Antimalarials – Glucose-6-phosphate dehydrogenase deficiency – Hematology – Malaria – Plasmodium – Primaquine – Quality control – Spectrophotometry
Zdroje
1. Lover AA, Baird JK, Gosling R, Price R. Malaria elimination: Time to target all species. Am J Trop Med Hyg. 2018. Epub 2018/05/16. doi: 10.4269/ajtmh.17-0869 29761762.
2. Baird JK, Battle KE, Howes RE. Primaquine ineligibility in anti-relapse therapy of Plasmodium vivax malaria: the problem of G6PD deficiency and cytochrome P-450 2D6 polymorphisms. Malar J. 2018;17:42. doi: 10.1186/s12936-018-2190-z PMC5778616. 29357870
3. Howes RE, Piel FB, Patil AP, Nyangiri OA, Gething PW, Dewi M, et al. G6PD deficiency prevalence and estimates of affected populations in malaria endemic countries: a geostatistical model-based map. PLoS Med. 2012;9(11):e1001339. doi: 10.1371/journal.pmed.1001339 23152723
4. 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, Molecules and Diseases. 2009;42(3):267–78. doi: 10.1016/j.bcmd.2008.12.005 19233695
5. Luzzatto L, Arese P. Favism and glucose-6-phosphate dehydrogenase deficiency. N Engl J Med. 2018;378(1):60–71. doi: 10.1056/nejmra1708111 29298156
6. Belfield KD, Tichy EM. Review and drug therapy implications of glucose-6-phosphate dehydrogenase deficiency. Am J Health Syst Pharm. 2018;75(3):97–104. doi: 10.2146/ajhp160961 29305344
7. Domingo GJ, Advani N, Satyagraha AW, Sibley CH, Rowley E, Kalnoky M, et al. Addressing the gender-knowledge gap in glucose-6-phosphate dehydrogenase deficiency: challenges and opportunities. Int Health. 2018;11(1):7–14. doi: doi.org/10.1093/inthealth/ihy060
8. Gómez-Manzo S, Marcial-Quino J, Vanoye-Carlo A, Serrano-Posada H, Ortega-Cuellar D, González-Valdez A, et al. Glucose-6-phosphate dehydrogenase: Update and analysis of new mutations around the world. Int J Mol Sci. 2016;17(12):2069. doi: 10.3390/ijms17122069 PMC5187869. 27941691
9. Minucci A, Moradkhani K, Hwang MJ, Zuppi C, Giardina B, Capoluongo E. Glucose-6-phosphate dehydrogenase (G6PD) mutations database: Review of the “old” and update of the new mutations. Blood Cells Mol Dis. 2012;48(3):154–65. doi: 10.1016/j.bcmd.2012.01.001 22293322
10. Luzzatto L. Glucose 6-phosphate dehydrogenase deficiency: from genotype to phenotype. Haematologica. 2006;91(10):1303. 17018377
11. Cunningham AD, Colavin A, Huang KC, Mochly-Rosen D. Coupling between protein stability and catalytic activity determines pathogenicity of G6PD variants. Cell Rep. 2017;18(11):2592–9. doi: 10.1016/j.celrep.2017.02.048 28297664
12. Ley B, Bancone G, von Seidlein L, Thriemer K, Richards JS, Domingo GJ, et al. Methods for the field evaluation of quantitative G6PD diagnostics: a review. Malar J. 2017;16(1):361. doi: 10.1186/s12936-017-2017-3 28893237
13. Pal S, Bansil P, Bancone G, Hrutkay S, Kahn M, Gornsawun G, et al. Evaluation of a novel quantitative test for glucose-6-phosphate dehydrogenase deficiency: bringing quantitative testing for glucose-6-phosphate dehydrogenase deficiency closer to the patient. Am J Trop Med Hyg. 2018:-. doi: 10.4269/ajtmh.18-0612 30350771
14. Alam MS, Kibria MG, Jahan N, Price RN, Ley B. Spectrophotometry assays to determine G6PD activity from Trinity Biotech and Pointe Scientific G6PD show good correlation. BMC Res Notes. 2018;11(1):855. doi: 10.1186/s13104-018-3964-7 30514365
15. Beutler E, Blume KG, Kaplan JC, Löhr GW, Ramot B, Valentine WN. International Committee for Standardization in Haematology: Recommended Methods for Red-Cell Enzyme Analysis. Br J Haematol. 1977;35(2):331–40. doi: 10.1111/j.1365-2141.1977.tb00589.x 857853
16. Domingo GJ, Satyagraha AW, Anvikar A, Baird K, Bancone G, Bansil P, et al. G6PD testing in support of treatment and elimination of malaria: recommendations for evaluation of G6PD tests. Malar J. 2013;12(1):391. doi: 10.1186/1475-2875-12-391 24188096
17. World Health Organization. Testing for G6PD deficiency for safe use of primaquine in radical cure of P. vivax and P. ovale malaria. Geneva: WHO, 2016.
18. Lacerda MVG, Llanos-Cuentas A, Krudsood S, Lon C, Saunders DL, Mohammed R, et al. Single-dose tafenoquine to prevent relapse of Plasmodium vivax malaria. N Engl J Med. 2019;380(3):215–28. doi: 10.1056/NEJMoa1710775 30650322
19. Llanos-Cuentas A, Lacerda MVG, Hien TT, Vélez ID, Namaik-larp C, Chu CS, et al. Tafenoquine versus primaquine to prevent relapse of Plasmodium vivax malaria. N Engl J Med. 2019;380(3):229–41. doi: 10.1056/NEJMoa1802537 30650326
20. Henriques G, Phommasone K, Tripura R, Peto TJ, Raut S, Snethlage C, et al. Comparison of glucose-6 phosphate dehydrogenase status by fluorescent spot test and rapid diagnostic test in Lao PDR and Cambodia. Malar J. 2018;17(1):243. doi: 10.1186/s12936-018-2390-6 29929514
21. Whiting PF, Rutjes AWS, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: A revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36. doi: 10.7326/0003-4819-155-8-201110180-00009 22007046
22. World Health Organization. Technical specifications series for submission to WHO prequalification–diagnostic assessment: in vitro diagnostic medical devices to identify glucose-6-phosphate dehydrogenase (G6PD) activity. Geneva: World Health Organization, 2016.
23. Wickham H. tidyverse: Easily install and load the ‘tidyverse’ 2017. R package version 1.2.1. Available from: https://CRAN.R-project.org/package=tidyverse
24. Wickham H. ggplot2: Elegant graphics for data analysis. New York: Springer-Verlag; 2009.
25. Wilke CO. cowplot: Streamlined plot theme and plot annotations for 'ggplot2' 2019. R package version 0.9.4. Available from: https://CRAN.R-project.org/package=cowplot
26. Stevenson M. epiR: Tools for the analysis of epidemiological data 2018. R package version 0.9–99. Available from: https://CRAN.R-project.org/package=epiR
27. R Core Team. R: A Language and Environment for Statistical Computing Vienna, Austria: R Foundation for Statistical Computing; 2018. Available from: https://www.R-project.org.
28. Bancone G, Chu CS, Chowwiwat N, Somsakchaicharoen R, Wilaisrisak P, Charunwatthana P, et al. Suitability of capillary blood for quantitative assessment of G6PD activity and performances of G6PD point-of-care tests. Am J Trop Med Hyg. 2015;92(4):818–24. Epub 2015/02/04. doi: 10.4269/ajtmh.14-0696 25646252; PubMed Central PMCID: PMC4385780.
29. Oo NN, Bancone G, Maw LZ, Chowwiwat N, Bansil P, Domingo GJ, et al. Validation of G6PD point-of-care rests among healthy volunteers in Yangon, Myanmar. PLoS ONE. 2016;11(4):e0152304–e. doi: 10.1371/journal.pone.0152304 27035821.
30. Satyagraha AW, Sadhewa A, Elvira R, Elyazar I, Feriandika D, Antonjaya U, et al. Assessment of point-of-care diagnostics for G6PD deficiency in malaria endemic rural Eastern Indonesia. PLoS Negl Trop Dis. 2016;10(2):e0004457. doi: 10.1371/journal.pntd.0004457 26894297
31. Travis SF, Kumar SP, Paez PC, Delivoria-Papadopoulos M. Red cell metabolic alterations in postnatal life in term infants. Glycolytic enzymes and glucose-6-phosphate dehydrogenase. Pediatr Res. 1980;14(12):1349. doi: 10.1203/00006450-198012000-00016 6451861
32. Yang W-C, Tai S, Hsu C-L, Fu C-M, Chou A-K, Shao P-L, et al. Reference levels for glucose-6-phosphate dehydrogenase enzyme activity in infants 7–90 days old in Taiwan. J Formos Med Assoc. 2019. https://doi.org/10.1016/j.jfma.2019.03.010.
33. Rueangweerayut R, Bancone G, Harrell EJ, Beelen AP, Kongpatanakul S, Mohrle JJ, et al. 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(3):702–11. Epub 2017/07/28. doi: 10.4269/ajtmh.16-0779 28749773.
34. Alam MS, Kibria MG, Jahan N, Thriemer K, Hossain MS, Douglas NM, et al. Field evaluation of quantitative point of care diagnostics to measure glucose-6-phosphate dehydrogenase activity. PLoS ONE. 2018;13(11):e0206331. doi: 10.1371/journal.pone.0206331 30388146
35. Major CA, Pretlow L, Fincher E, Koziatek V. Validating the assessment of glucose-6-phosphate dehydrogenase (G6PD). Clin Lab Sci. 2006;19(3):134–9. 16910228
36. WHO Working Group. Glucose-6-phosphate dehydrogenase deficiency. Bull World Health Organ. 1989;67(6):601–11. PMC2491315. 2633878
37. Commons RJ, McCarthy JS, Price RN. Tafenoquine for the radical cure and prevention of malaria: the importance of testing for G6PD deficiency. Med J Aust. 2020;212(4):152–3.e1.
38. 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 of Trop Med Public Health. 2014;45(1):187–93. Epub 2014/06/27. 24964669.
39. Roh ME, Oyet C, Orikiriza P, Wade M, Mwanga-Amumpaire J, Boum Y 2nd, et al. Screening for glucose-6-phosphate dehydrogenase deficiency using three detection methods: A cross-sectional survey in Southwestern Uganda. Am J Trop Med Hyg. 2016;95(5):1094–9. doi: 10.4269/ajtmh.16-0552 27672207.
Článek vyšel v časopise
PLOS Medicine
2020 Číslo 5
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- „Jednohubky“ z klinického výzkumu – 2024/44
- Je libo čepici místo mozkového implantátu?
Nejčtenější v tomto čísle
- National and regional prevalence of posttraumatic stress disorder in sub-Saharan Africa: A systematic review and meta-analysis
- Risk of severe maternal morbidity or death in relation to elevated hemoglobin A1c preconception, and in early pregnancy: A population-based cohort study
- Antibody-based therapies for COVID-19: Can Europe move faster?
- The association of innate and adaptive immunity, subclinical atherosclerosis, and cardiovascular disease in the Rotterdam Study: A prospective cohort study
