Performance of the Access Bio/CareStart rapid diagnostic test for the detection of glucose-6-phosphate dehydrogenase deficiency: A systematic review and meta-analysis

English version

Autoři: Benedikt Ley ^aff001; Ari Winasti Satyagraha ^aff002; Hisni Rahmat ^aff002; Michael E. von Fricken ^aff003; Nicholas M. Douglas ^aff001; Daniel A. Pfeffer ^aff001; Fe Espino ^aff004; Lorenz von Seidlein ^aff005; Gisela Henriques ^aff007; Nwe Nwe Oo ^aff008; Didier Menard ^aff009; Sunil Parikh ^aff010; Germana Bancone ^aff006; Amalia Karahalios ^aff012; Ric N. Price ^aff001
Působiště autorů: Global and Tropical Health Division, Menzies School of Health Research and Charles Darwin University, Darwin, Australia ^aff001; Eijkman Institute for Molecular Biology, Jakarta, Indonesia ^aff002; Department of Global and Community Health, George Mason University, Fairfax, Virginia, United States of America ^aff003; Research Institute for Tropical Medicine, Department of Health, Muntinlupa City, Philippines ^aff004; Mahidol-Oxford Tropical Medicine Research Unit (MORU), Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand ^aff005; Centre for Tropical Medicine and Global Health, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, United Kingdom ^aff006; Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom ^aff007; Department of Medical Research (Lower Myanmar), Yangon, Republic of the Union of Myanmar ^aff008; Malaria Genetics and Resistance Unit, Institut Pasteur, Paris, France ^aff009; Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, Connecticut, United States of America ^aff010; Shoklo Malaria Research Unit, Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, Thailand ^aff011; Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, Australia ^aff012
Vyšlo v časopise: Performance of the Access Bio/CareStart rapid diagnostic test for the detection of glucose-6-phosphate dehydrogenase deficiency: A systematic review and meta-analysis. PLoS Med 16(12): e1002992. doi:10.1371/journal.pmed.1002992
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1002992

Souhrn

Background

To reduce the risk of drug-induced haemolysis, all patients should be tested for glucose-6-phosphate dehydrogenase (G6PD) deficiency (G6PDd) prior to prescribing primaquine (PQ)-based radical cure for the treatment of vivax malaria. This systematic review and individual patient meta-analysis assessed the utility of a qualitative lateral flow assay from Access Bio/CareStart (Somerset, NJ) (CareStart Screening test for G6PD deficiency) for the diagnosis of G6PDd compared to the gold standard spectrophotometry (International Prospective Register of Systematic Reviews [PROSPERO]: CRD42019110994).

Methods and findings

Articles published on PubMed between 1 January 2011 and 27 September 2019 were screened. Articles reporting performance of the standard CSG from venous or capillary blood samples collected prospectively and considering spectrophotometry as gold standard (using kits from Trinity Biotech PLC, Wicklow, Ireland) were included. Authors of articles fulfilling the inclusion criteria were contacted to contribute anonymized individual data. Minimal data requested were sex of the participant, CSG result, spectrophotometry result in U/gHb, and haemoglobin (Hb) reading. The adjusted male median (AMM) was calculated per site and defined as 100% G6PD activity. G6PDd was defined as an enzyme activity of less than 30%. Pooled estimates for sensitivity and specificity, unconditional negative predictive value (NPV), positive likelihood ratio (LR+), and negative likelihood ratio (LR−) were calculated comparing CSG results to spectrophotometry using a random-effects bivariate model.

Of 11 eligible published articles, individual data were available from 8 studies, 6 from Southeast Asia, 1 from Africa, and 1 from the Americas. A total of 5,815 individual participant data (IPD) were available, of which 5,777 results (99.3%) were considered for analysis, including data from 3,095 (53.6%) females. Overall, the CSG had a pooled sensitivity of 0.96 (95% CI 0.90–0.99) and a specificity of 0.95 (95% CI 0.92–0.96). When the prevalence of G6PDd was varied from 5% to 30%, the unconditional NPV was 0.99 (95% CI 0.94–1.00), with an LR+ and an LR− of 18.23 (95% CI 13.04–25.48) and 0.05 (95% CI 0.02–0.12), respectively.

Performance was significantly better in males compared to females (p = 0.027) but did not differ significantly between samples collected from capillary or venous blood (p = 0.547). Limitations of the study include the lack of wide geographical representation of the included data and that the CSG results were generated under research conditions, and therefore may not reflect performance in routine settings.

Conclusions

The CSG performed well at the 30% threshold. Its high NPV suggests that the test is suitable to guide PQ treatment, and the high LR+ and low LR− render the test suitable to confirm and exclude G6PDd. Further operational studies are needed to confirm the utility of the test in remote endemic settings.

Klíčová slova:

Blood – Spectrophotometry – Systematic reviews – Malaria – Glucose-6-phosphate dehydrogenase deficiency – Blood counts – Capillaries

Zdroje

1. Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM. Vivax malaria: neglected and not benign. The American journal of tropical medicine and hygiene. 2007;77(6 Suppl):79–87. 18165478

2. Recht J, Ashley EA, White NJ. Use of primaquine and glucose-6-phosphate dehydrogenase deficiency testing: Divergent policies and practices in malaria endemic countries. PLoS neglected tropical diseases. 2018;12(4):e0006230. doi: 10.1371/journal.pntd.0006230 29672516

3. ARMY giving primaquine treatment to all returning servicemen. Public Health Rep. 1952;67(2):178–9. 14900346

4. WHO. Guidelines for the treatment of malaria - 3rd Edition. Switzerland: WHO; 2015.

5. John GK, Douglas NM, von Seidlein L, Nosten F, Baird JK, White NJ, et al. Primaquine radical cure of Plasmodium vivax: a critical review of the literature. Malaria journal. 2012;11:280. doi: 10.1186/1475-2875-11-280 22900786

6. Baird JK, Hoffman SL. Primaquine therapy for malaria. Clin Infect Dis. 2004;39(9):1336–45. doi: 10.1086/424663 15494911

7. Ashley EA, Recht J, White NJ. Primaquine: the risks and the benefits. Malaria journal. 2014;13:418. doi: 10.1186/1475-2875-13-418 25363455

8. Commons RJ, Simpson JA, Thriemer K, Humphreys GS, Abreha T, Alemu SG, et al. The effect of chloroquine dose and primaquine on Plasmodium vivax recurrence: a WorldWide Antimalarial Resistance Network systematic review and individual patient pooled meta-analysis. The Lancet Infectious diseases. 2018;18(9):1025–34. doi: 10.1016/S1473-3099(18)30348-7 30033231

9. WHO. Guide to G6PD deficiency rapid diagnostic testing to support P. vivax radical cure. In: Organization WH, editor. Geneva, switzerland2018.

10. Gomez-Manzo S, Marcial-Quino J, Vanoye-Carlo A, Serrano-Posada H, Ortega-Cuellar D, Gonzalez-Valdez A, et al. Glucose-6-Phosphate Dehydrogenase: Update and Analysis of New Mutations around the World. Int J Mol Sci. 2016;17(12).

11. 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

12. Luzzatto L. Glucose 6-phosphate dehydrogenase deficiency: from genotype to phenotype. Haematologica. 2006;91(10):1303–6. 17018377

13. Chu CS, Bancone G, Moore KA, Win HH, Thitipanawan N, Po C, et al. Haemolysis in G6PD Heterozygous Females Treated with Primaquine for Plasmodium vivax Malaria: A Nested Cohort in a Trial of Radical Curative Regimens. PLoS medicine. 2017;14(2):e1002224. doi: 10.1371/journal.pmed.1002224 28170391

14. Chu CS, Bancone G, Nosten F, White NJ, Luzzatto L. Primaquine-induced haemolysis in females heterozygous for G6PD deficiency. Malaria journal. 2018;17(1):101. doi: 10.1186/s12936-018-2248-y 29499733

15. von Seidlein L, Auburn S, Espino F, Shanks D, Cheng Q, McCarthy J, et al. Review of key knowledge gaps in glucose-6-phosphate dehydrogenase deficiency detection with regard to the safe clinical deployment of 8-aminoquinoline treatment regimens: a workshop report. Malaria journal. 2013;12:112. doi: 10.1186/1475-2875-12-112 23537118

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. Malaria journal. 2013;12:391. doi: 10.1186/1475-2875-12-391 24188096

17. Ley B, Luter N, Espino FE, Devine A, Kalnoky M, Lubell Y, et al. The challenges of introducing routine G6PD testing into radical cure: a workshop report. Malaria journal. 2015;14:377. doi: 10.1186/s12936-015-0896-8 26416229

18. Beutler E. Glucose-6-phosphate dehydrogenase deficiency: a historical perspective. Blood. 2008;111(1):16–24. doi: 10.1182/blood-2007-04-077412 18156501

19. Kim S, Nguon C, Guillard B, Duong S, Chy S, Sum S, et al. Performance of the CareStart G6PD deficiency screening test, a point-of-care diagnostic for primaquine therapy screening. PloS one. 2011;6(12):e28357. doi: 10.1371/journal.pone.0028357 22164279

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. Malaria journal. 2018;17(1):243. doi: 10.1186/s12936-018-2390-6 29929514

21. 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. The American journal of tropical medicine and hygiene. 2015;92(4):818–24. doi: 10.4269/ajtmh.14-0696 25646252

22. Banoo S, Bell D, Bossuyt P, Herring A, Mabey D, Poole F, et al. Evaluation of diagnostic tests for infectious diseases: general principles. Nature reviews Microbiology. 2006;4(12 Suppl):S20–32. doi: 10.1038/nrmicro1570 17366684

23. 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. Malaria journal. 2017;16(1):361. doi: 10.1186/s12936-017-2017-3 28893237

24. Riley RD, Dodd SR, Craig JV, Thompson JR, Williamson PR. Meta-analysis of diagnostic test studies using individual patient data and aggregate data. Statistics in medicine. 2008;27(29):6111–36. doi: 10.1002/sim.3441 18816508

25. 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 medicine. 2012;9(11):e1001339. doi: 10.1371/journal.pmed.1001339 23152723

26. McGee S. Simplifying likelihood ratios. J Gen Intern Med. 2002;17(8):646–9. doi: 10.1046/j.1525-1497.2002.10750.x 12213147

27. Simundic AM. Measures of Diagnostic Accuracy: Basic Definitions. EJIFCC. 2009;19(4):203–11. 27683318

28. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Annals of internal medicine. 2011;155(8):529–36. doi: 10.7326/0003-4819-155-8-201110180-00009 22007046

29. Espino FE, Bibit JA, Sornillo JB, Tan A, von Seidlein L, Ley B. Comparison of Three Screening Test Kits for G6PD Enzyme Deficiency: Implications for Its Use in the Radical Cure of Vivax Malaria in Remote and Resource-Poor Areas in the Philippines. PloS one. 2016;11(2):e0148172. doi: 10.1371/journal.pone.0148172 26849445

30. Oo NN, Bancone G, Maw LZ, Chowwiwat N, Bansil P, Domingo GJ, et al. Validation of G6PD Point-of-Care Tests among Healthy Volunteers in Yangon, Myanmar. PloS one. 2016;11(4):e0152304. doi: 10.1371/journal.pone.0152304 27035821

31. Roca-Feltrer A, Khim N, Kim S, Chy S, Canier L, Kerleguer A, et al. Field trial evaluation of the performances of point-of-care tests for screening G6PD deficiency in Cambodia. PloS one. 2014;9(12):e116143. doi: 10.1371/journal.pone.0116143 25541721

32. 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 neglected tropical diseases. 2016;10(2):e0004457. doi: 10.1371/journal.pntd.0004457 26894297

33. 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. The American journal of tropical medicine and hygiene. 2016;95(5):1094–9. doi: 10.4269/ajtmh.16-0552 27672207

34. von Fricken ME, Weppelmann TA, Eaton WT, Masse R, Beau de Rochars MV, Okech BA. Performance of the CareStart glucose-6-phosphate dehydrogenase (G6PD) rapid diagnostic test in Gressier, Haiti. The American journal of tropical medicine and hygiene. 2014;91(1):77–80. doi: 10.4269/ajtmh.14-0100 24778197

35. Brito MA, Peixoto HM, Almeida AC, Oliveira MR, Romero GA, Moura-Neto JP, et al. Validation of the rapid test Carestart(tm) G6PD among malaria vivax-infected subjects in the Brazilian Amazon. Rev Soc Bras Med Trop. 2016;49(4):446–55. doi: 10.1590/0037-8682-0134-2016 27598631

36. Abdul-Ghani R, Mahdy MA, Saif-Ali R, Alkubati SA, Alqubaty AR, Al-Mikhlafy AA, et al. Glucose-6-phosphate dehydrogenase deficiency among Yemeni children residing in malaria-endemic areas of Hodeidah governorate and evaluation of a rapid diagnostic test for its detection. Malaria journal. 2016;15:327. doi: 10.1186/s12936-016-1372-9 27329471

37. Adu-Gyasi D, Asante KP, Newton S, Dosoo D, Amoako S, Adjei G, et al. Evaluation of the diagnostic accuracy of CareStart G6PD deficiency Rapid Diagnostic Test (RDT) in a malaria endemic area in Ghana, Africa. PloS one. 2015;10(4):e0125796. doi: 10.1371/journal.pone.0125796 25885097

38. Baird JK, Dewi M, Subekti D, Elyazar I, Satyagraha AW. Noninferiority of glucose-6-phosphate dehydrogenase deficiency diagnosis by a point-of-care rapid test vs the laboratory fluorescent spot test demonstrated by copper inhibition in normal human red blood cells. Transl Res. 2015;165(6):677–88. doi: 10.1016/j.trsl.2014.09.009 25312015

39. 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

40. Ebstie YA, Abay SM, Tadesse WT, Ejigu DA. Tafenoquine and its potential in the treatment and relapse prevention of Plasmodium vivax malaria: the evidence to date. Drug Des Devel Ther. 2016;10:2387–99. doi: 10.2147/DDDT.S61443 27528800

41. Devine A, Parmiter M, Chu CS, Bancone G, Nosten F, Price RN, et al. Using G6PD tests to enable the safe treatment of Plasmodium vivax infections with primaquine on the Thailand-Myanmar border: A cost-effectiveness analysis. PLoS neglected tropical diseases. 2017;11(5):e0005602. doi: 10.1371/journal.pntd.0005602 28542194

42. Robinson KM, Yang W, Haidar CE, Hankins JS, Jay DW, Kornegay N, et al. Concordance between glucose-6-phosphate dehydrogenase (G6PD) genotype and phenotype and rasburicase use in patients with hematologic malignancies. Pharmacogenomics J. 2019;19(3):305–14. doi: 10.1038/s41397-018-0043-3 30206300

43. Shah SS, Macharia A, Makale J, Uyoga S, Kivinen K, Craik R, et al. Genetic determinants of glucose-6-phosphate dehydrogenase activity in Kenya. BMC Med Genet. 2014;15:93. doi: 10.1186/s12881-014-0093-6 25201310

44. Johnson MK, Clark TD, Njama-Meya D, Rosenthal PJ, Parikh S. Impact of the method of G6PD deficiency assessment on genetic association studies of malaria susceptibility. PloS one. 2009;4(9):e7246. doi: 10.1371/journal.pone.0007246 19789650

45. 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