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Performance of a Commercial Multiplex Allele-Specific Polymerase Chain Reaction Kit to Genotype African-Type Glucose-6-Phosphate Dehydrogenase Deficiency
Oum Kelthoum Mamadou Djigo
Oum Kelthoum Mamadou Djigo
Unité de Recherche “Génomes et Milieux” (Jeune Equipe Associée à l’Institut de Recherche pour le Développement), Faculté des Sciences et Techniques, Université de Nouakchott, Nouakchott, Mauritania;
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Nicolas Gomez
Nicolas Gomez
Aix Marseille Université, Institut de Recherche pour le Développement, Assistance Publique-Hôpitaux de Marseille, Service de Santé des Armées, Vecteurs–Infections Tropicales et Méditerranéennes, Marseille, France;
Institut Hospitalo-Universitaire–Méditerranée Infection, Marseille, France;
Unité de Parasitologie Entomologie, Département de Microbiologie et Maladies Infectieuses, Institut de Recherche Biomédicale des Armées, Marseille, France
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Institut Hospitalo-Universitaire–Méditerranée Infection, Marseille, France;
Unité de Parasitologie Entomologie, Département de Microbiologie et Maladies Infectieuses, Institut de Recherche Biomédicale des Armées, Marseille, France
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Mohamed Salem Ould Ahmedou Salem
Mohamed Salem Ould Ahmedou Salem
Unité de Recherche “Génomes et Milieux” (Jeune Equipe Associée à l’Institut de Recherche pour le Développement), Faculté des Sciences et Techniques, Université de Nouakchott, Nouakchott, Mauritania;
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Leonardo Basco
Leonardo Basco
Aix Marseille Université, Institut de Recherche pour le Développement, Assistance Publique-Hôpitaux de Marseille, Service de Santé des Armées, Vecteurs–Infections Tropicales et Méditerranéennes, Marseille, France;
Institut Hospitalo-Universitaire–Méditerranée Infection, Marseille, France;
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Institut Hospitalo-Universitaire–Méditerranée Infection, Marseille, France;
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Ali Ould Mohamed Salem Boukhary
Ali Ould Mohamed Salem Boukhary
Unité de Recherche “Génomes et Milieux” (Jeune Equipe Associée à l’Institut de Recherche pour le Développement), Faculté des Sciences et Techniques, Université de Nouakchott, Nouakchott, Mauritania;
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Sébastien Briolant
Sébastien Briolant
Aix Marseille Université, Institut de Recherche pour le Développement, Assistance Publique-Hôpitaux de Marseille, Service de Santé des Armées, Vecteurs–Infections Tropicales et Méditerranéennes, Marseille, France;
Institut Hospitalo-Universitaire–Méditerranée Infection, Marseille, France;
Unité de Parasitologie Entomologie, Département de Microbiologie et Maladies Infectieuses, Institut de Recherche Biomédicale des Armées, Marseille, France
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ABSTRACT.
8-Aminoquinoline antimalarial drugs (primaquine, tafenoquine) are required for complete cure of Plasmodium vivax malaria, but they are contraindicated in patients with glucose-6-phosphate dehydrogenase (G6PD) deficiency. In the absence of spectrophotometry, which is a gold standard for measuring G6PD activity, G6PD genotyping is one of the alternatives to establish a database and distribution map of G6PD enzyme deficiency in Mauritania, which has become a new epicenter of P. vivax malaria in West Africa. The aim of our study was to assess the performance of multiplex allele-specific polymerase chain reaction (PCR) (African-type Diaplex C™ G6PD kit) against PCR–restriction fragment length polymorphism and sequencing. Of 146 mutations associated with G6PD A− genotypes in 177 blood samples from Mauritanian patients, all but two samples were identified correctly using multiplex allele-specific PCR (100% sensitivity and 99% specificity; “almost perfect agreement” between allele-specific PCR and PCR-restriction fragment length polymorphism/sequencing, with a kappa coefficient of 0.977). Despite a suboptimal PCR protocol for dried blood spots and the inability of the commercial assay to predict unequivocally the G6PD enzyme level in heterozygous females, the African-type Diaplex C™ G6PD genotyping kit seemed to be a valuable screening tool for male subjects and for research purposes in resource-limited countries where spectrophotometer and DNA sequencing are not available.
Author Notes
Financial support: This research was funded by Institut de Recherche pour le Développement (IRD) (grant Jeune Equipe Associée à l’IRD) and the Direction Générale de l’Armement (grant no. PDH-2-NRBC-2-B-2113). O. K. M. D. received a PhD grant from the French government.
Disclosure: The funding sources of this study had no role in study and protocol design, data collection, analysis, or data interpretation.
Disclaimer: The opinions and views expressed in this publication are those of the authors and do not necessarily reflect the official policy, views, or position of the Direction Générale de l’Armement, French Army Institute of Biomedical Research, French Service de Santé des Armées, Aix-Marseille University. The testing of the commercial products mentioned in this publication does not imply endorsement by the French government institutions or semi-private institutions.
Authors’ addresses: Oum Kelthoum Mamadou Djigo, Mohamed Salem Ould Ahmedou Salem, and Ali Ould Mohamed Salem Boukhary, Unité de Recherche “Génomes et Milieux” (Jeune Equipe Associée à l’Institut de Recherche pour le Développement), Faculté des Sciences et Techniques, Université de Nouakchott, Nouakchott, Mauritania, E-mails: mari1702@live.fr, salem0606@yahoo.fr, and alimedsalem@gmail.com. Nicolas Gomez and Sébastien Briolant, Aix Marseille Université, Institut de Recherche pour le Développement, Assistance Publique-Hôpitaux de Marseille, Service de Santé des Armées, Vecteurs–Infections Tropicales et Méditerranéennes, Marseille, France, Institut Hospitalo-Universitaire–Méditerranée Infection, Marseille, France, and Unité de Parasitologie Entomologie, Département de Microbiologie et Maladies Infectieuses, Institut de Recherche Biomédicale des Armées, Marseille, France, E-mails: nico13dna@hotmail.com and sbriolant@wanadoo.fr. Leonardo Basco, Aix Marseille Université, Institut de Recherche pour le Développement, Assistance Publique-Hôpitaux de Marseille, Service de Santé des Armées, Vecteurs–Infections Tropicales et Méditerranéennes, Marseille, France, and Institut Hospitalo-Universitaire–Méditerranée Infection, Marseille, France, E-mail: lkbasco@yahoo.fr.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization , 2020. World Malaria Report 2020: 20 Years of Global Progress and Challenges. Geneva, Switzerland: WHO. Available at: https://www.who.int/publications/i/item/9789240015791. Accessed March 22, 2022.
-
2.
Lekweiry KM, Salem MSOA, Basco LK, Briolant S, Hafid J, Boukhary AOMS, 2015. Malaria in Mauritania: retrospective and prospective overview. Malar J 14: 100.
-
3.
Ould Ahmedou Salem MS, Mint Lekweiry K, Mint Deida J, Ould Emouh A, Ould Weddady M, Ould Mohamed Salem Boukhary A, Basco LK, 2015. Increasing prevalence of Plasmodium vivax among febrile patients in Nouakchott, Mauritania. Am J Trop Med Hyg 92: 537–540.
-
4.
Mint Deida J, Ould Khalef Y, Mint Semane E, Ould Ahmedou Salem MS, Bogreau H, Basco L, Ould Mohamed Salem Boukhary A, Tahar R, 2018. Assessment of drug resistance associated genetic diversity in Mauritanian isolates of Plasmodium vivax reveals limited polymorphism. Malar J 17: 416.
-
5.
Deida J, Tahar R, Khalef YO, Lekweiry KM, Hmeyade A, Khairy MLO, Simard F, Bogreau H, Basco L, Boukhary AOMS, 2019. Oasis malaria, northern Mauritania. Emerg Infect Dis 25: 273–280.
-
6.
Diallo SM, Bogreau H, Papa Mze N, Ould Ahmedou Salem MS, Ould Khairy ML, Parola P, Basco L, Ould Mohamed Salem Boukhary A, 2020. Malaria epidemiology in Kobeni department, southeastern Mauritania from 2015 to 2017. Infect Dis Poverty 9: 21.
-
7.
Ould Ahmedou Salem MS, Basco LK, Ouldabdallahi M, Mint Lekweiry K, Konaté L, Faye O, Ould Mohamed Salem Boukhary A, 2015. Malaria-associated morbidity during the rainy season in Saharan and Sahelian zones in Mauritania. Acta Trop 152: 1–7.
-
8.
Ba H, Duffy CW, Ahouidi AD, Deh YB, Diallo MY, Tandia A, Conway DJ, 2016. Widespread distribution of Plasmodium vivax malaria in Mauritania on the interface of the Maghreb and West Africa. Malar J 15: 80.
-
9.
Ba H et al., 2020. Multi-locus genotyping reveals established endemicity of a geographically distinct Plasmodium vivax population in Mauritania, West Africa. PLoS Negl Trop Dis 14: e0008945.
-
10.
World Health Organization Regional Office for the Eastern Mediterranean and Moroccan Ministry of Health , 2007. Malaria in Morocco: Relentless Efforts Towards the Goal of Elimination. Available at: https://apps.who.int/iris/handle/10665/116532. Accessed March 22, 2022.
-
11.
World Health Organization , 2010. Morocco certified malaria-free. Wkly Epidemiol Rec 85: 235–236.
-
12.
World Health Organization , 2019. The E-2020 Initiative of 21 Malaria-Eliminating Countries: 2019 Progress Report. Available at: https://apps.who.int/iris/handle/10665/325304?locale-attribute=fr&. Accessed March 22, 2022.
-
13.
World Health Organization , 2018. World Malaria Report 2018: Country Profiles. Available at: https://www.who.int/publications/i/item/9789241565653. Accessed March 22, 2022.
-
14.
Bernabeu M et al., 2012. Plasmodium vivax malaria in Mali: a study from three different regions. Malar J 11: 405.
-
15.
Koita OA et al., 2012. Effect of seasonality and ecological factors on the prevalence of the four malaria parasite species in northern Mali. J Trop Med 2012: 367160. doi:10.1155/2012/367160.
-
16.
Niang M et al., 2015. A molecular survey of acute febrile illnesses reveals Plasmodium vivax infections in Kedougou, southeastern Senegal. Malar J 14: 281.
-
17.
Williams J et al., 2016. Non-falciparum malaria infections in pregnant women in West Africa. Malar J 15: 53.
-
18.
Niang M, Diop F, Niang O, Sadio BD, Sow A, Faye O, Diallo M, Sall AA, Perraut R, Toure-Balde A, 2017. Unexpected high circulation of Plasmodium vivax in asymptomatic children from Kédougou, southeastern Senegal. Malar J 16: 497.
-
19.
Niangaly A et al., 2017. Plasmodium vivax infections over 3 years in Duffy blood group negative Malians in Bandiagara, Mali. Am J Trop Med Hyg 97: 744–752.
-
20.
Ould Ahmedou Salem MS et al., 2015. Efficacy of chloroquine for the treatment of Plasmodium vivax in the Saharan zone in Mauritania. Malar J 14: 39.
-
21.
Recht J, Ashley E, White N, 2014. Safety of 8-Aminoquinoline Antimalarial Medicines. Available at: https://apps.who.int/iris/handle/10665/112735. Accessed March 22, 2022.
-
22.
World Health Organization , 2015. Guidelines for the Treatment of Malaria, 3rd Ed. Available at: https://apps.who.int/iris/handle/10665/162441. Accessed March 22, 2022.
-
23.
Baird JK, 2019. 8-Aminoquinoline therapy for latent malaria. Clin Microbiol Rev 32: e00011–e00019.
-
24.
Hounkpatin AB, Kreidenweiss A, Held J, 2019. Clinical utility of tafenoquine in the prevention of relapse of Plasmodium vivax malaria: a review on the mode of action and emerging trial data. Infect Drug Resist 12: 553–570.
-
25.
Mauritanian Ministry of Health , 2013. Guide Clinique et Thérapeutique à l’Usage du Personnel des Centres de Santé de la Mauritanie. Available at: http://www.sante.gov.mr/?wpfb_dl=140. Accessed March 22, 2022.
-
26.
Ashley EA, Recht J, White NJ, 2014. Primaquine: the risks and the benefits. Malar J 13: 418.
-
27.
Briolant S, Pradines B, Basco LK, 2017. Role of primaquine in malaria control and elimination in French-speaking Africa. Bull Soc Pathol Exot 110: 198–206.
-
28.
World Health Organization , 2016. Testing for G6PD Deficiency for Safe Use of Primaquine in Radical Cure of P. vivax and P. ovale Malaria: Policy Brief. Available at: https://apps.who.int/iris/handle/10665/250297?locale-attribute=fr&. Accessed March 22, 2022.
-
29.
Ley B, Bancone G, von Seidlein L, Thriemer K, Richards JS, Domingo GJ, Price RN, 2017. Methods for the field evaluation of quantitative G6PD diagnostics: a review. Malar J 16: 361.
-
30.
Grobusch MP, Rodríguez-Morales AJ, Schlagenhauf P, 2019. The primaquine problem: and the solution? Point-of-care diagnostics for glucose 6-phosphate dehydrogenase deficiency. Clin Infect Dis 69: 1443–1445.
-
31.
Pfeffer DA et al., 2020. Quantification of glucose-6-phosphate dehydrogenase activity by spectrophotometry: a systematic review and meta-analysis. PLoS Med 17: e1003084.
-
32.
Vulliamy TJ, D’Urso M, Battistuzzi G, Estrada M, Foulkes NS, Martini G, Calabro V, Poggi V, Giordano R, Town M, 1988. Diverse point mutations in the human glucose-6-phosphate dehydrogenase gene cause enzyme deficiency and mild or severe hemolytic anemia. Proc Natl Acad Sci USA 85: 5171–5175.
-
33.
Nkhoma ET, Poole C, Vannappagari V, Hall SA, Beutler E, 2009. The global prevalence of glucose-6-phosphate dehydrogenase deficiency: a systematic review and meta-analysis. Blood Cells Mol Dis 42: 267–278.
-
34.
Gómez-Manzo S et al., 2014. The stability of G6PD is affected by mutations with different clinical phenotypes. Int J Mol Sci 15: 21179–21201.
-
35.
Minucci A, Moradkhani K, Hwang MJ, Zuppi C, Giardina B, Capoluongo E, 2012. Glucose-6-phosphate dehydrogenase (G6PD) mutations database: review of the “old” and update of the new mutations. Blood Cells Mol Dis 48: 154–165.
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