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G6PD Deficiency in Latin America: Systematic Review on Prevalence and Variants

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G6PD Deficiency in Latin America: Systematic Review on Prevalence and Variants Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 109(5): 553-568, August 2014 553 G6PD deficiency in Latin America: systematic review on prevalence and variants Wuelton M Monteiro1,2/+, Fernando FA Val1,2, André M Siqueira1,2, Gabriel P Franca1, Vanderson S Sampaio1,2, Gisely C Melo1,2, Anne CG Almeida1,2, Marcelo AM Brito1,2, Henry M Peixoto3, Douglas Fuller4, Quique Bassat5, Gustavo AS Romero3,6, Maria Regina F Oliveira3,6, Marcus Vinícius G Lacerda1,2 1Gerência de Malária, Fundação de Medicina Tropical Dr Heitor Vieira Dourado, Manaus, AM, Brasil 2Escola Superior de Ciências da Saúde, Universidade do Estado do Amazonas, Manaus, AM, Brasil 3Faculdade de Medicina, Universidade de Brasília, Brasília, DF, Brasil 4Department of Geography and Regional Studies, University of Miami, Coral Gables, FL, USA 5Barcelona Centre for International Health Research, Hospital Clinic, University of Barcelona, Barcelona, Spain 6Instituto Nacional de Ciência e Tecnologia para Avaliação de Tecnologias em Saúde, Porto Alegre, RS, Brasil Plasmodium vivax radical cure requires the use of primaquine (PQ), a drug that induces haemolysis in glucose- 6-phosphate dehydrogenase deficient (G6PDd) individuals, which further hampers malaria control efforts. The aim of this work was to study the G6PDd prevalence and variants in Latin America (LA) and the Caribbean region. A sys- tematic search of the published literature was undertaken in August 2013. Bibliographies of manuscripts were also searched and additional references were identified. Low prevalence rates of G6PDd were documented in Argentina, Bolivia, Mexico, Peru and Uruguay, but studies from Curaçao, Ecuador, Jamaica, Saint Lucia, Suriname and Trini- dad, as well as some surveys carried out in areas of Brazil, Colombia and Cuba, have shown a high prevalence (> 10%) of G6PDd. The G6PD A-202A mutation was the variant most broadly distributed across LA and was identified in 81.1% of the deficient individuals surveyed. G6PDd is a frequent phenomenon in LA, although certain Amerindian populations may not be affected, suggesting that PQ could be safely used in these specific populations. Population- wide use of PQ as part of malaria elimination strategies in LA cannot be supported unless a rapid, accurate and field-deployable G6PDd diagnostic test is made available. Key words: G6PD deficiency - malaria control - Plasmodium vivax - primaquine - haemolysis - Amerindians Glucose-6-phosphate dehydrogenase (G6PD) is a cy- stressors, e.g., diabetic ketoacidosis, drugs, pathogens toplasmic enzyme. The major function of G6PD is the or types of food, causing syndromes such as acute hae- prevention of oxidative damage to cells by promoting molytic anaemia (AHA), neonatal jaundice (NNJ) and detoxification of free radicals. This metabolic pathway congenital non-spherocytic haemolytic anaemia, with involves the production of nicotinamide adenine dinu- the resulting manifestations depending on the amount of cleotide phosphate (NADPH), which participates in the oxidative stress experienced in the cells and the levels of glutathione (GSH) cycle, protecting the cell against hy- enzyme activity (Mason et al. 2007). drogen peroxide-induced damage and assuring an oxida- G6PDd is found worldwide with varying frequen- tive balance profile within the cell (Cappellini & Fiorelli cies depending on the region and ethnic group. The 2008). The G6PD gene presents an X-linked pattern overall G6PDd allele frequency across malaria endemic (Beutler 1994), where hemizygous males and homozy- countries is estimated to be 8%, corresponding to ap- gous females are deficient and heterozygous females proximately 220 million males and 133 million females may or may not be deficient because of mosaicism. (Howes et al. 2012). Variable enzyme activity levels have Despite the majority of G6PD deficient (G6PDd) indi- been measured among deficient individuals based on the viduals being asymptomatic, some present haemolytic diversity of mutations. The World Health Organization incidents that may be triggered by intrinsic or extrinsic (WHO) has classifies G6PDd according to enzyme ac- tivity, ranging from ≤ 1% to over 150%, classes I-V, re- spectively, in which classes I, II and III are considered at risk for haemolytic events (WHO 1989). The highest G6PDd prevalence has been found to occur in sub-Saha- ran Africa and the Arabian Peninsula (Howes et al. 2012). doi: 10.1590/0074-0276140123 Recent data found 186 known G6PD genotypic variants, Financial support: CNPq, PRONEX Malaria (575788/2008-9), most of them resulting in phenotypes that are asymp- FAPEAM (HEMOVIVAX) (1027/2011 and 3140/2012) tomatic until exposed to haemolytic triggers (Minucci GASR received a visiting fellowship from the FAPEAM (PECTI- et al. 2012). These G6PD variants are heterogeneously SAÚDE), QB has a fellowship from the program Miguel Servet of the ISCIII (CP11/00269), MVGL has a Level 1 fellowship from the CNPq. spread among different countries, presenting distinct + Corresponding author: [email protected] region-specific distributions (Howes et al. 2013), which Received 9 April 2014 could be related to specific routes of human migration. Accepted 2 July 2014 Among all the known deficiencies, the G6PD A- and the online | memorias.ioc.fiocruz.br 554 G6PD deficiency in Latin America • Wuelton M Monteiro et al. G6PD Mediterranean variants have been reported to be Argentina and Paraguay have been classified as malaria- detected more frequently in certain populations and are eliminating countries. The remaining countries are still the variants primarily responsible for the occurrence of in the phase of controlling transmission (WHO 2012a). haemolytic events (Frank 2005). The G6PD A- variant Predominance of P. vivax malaria in these countries is es- is the most predominant allele in the African continent, pecially relevant given that radical cure requires the use of whereas the G6PD Mediterranean allele is more frequent PQ, implying a risk of haemolysis and its adverse conse- in Western Asia (Howes et al. 2013). quences in G6PDd individuals (Beutler & Duparc 2007). Malaria in humans is predominantly caused by two The public health consequences of this condition deserve Plasmodia species, Plasmodium falciparum and Plasmo- special attention because of the impossibility of using PQ dium vivax and is estimated to be spread over more than in regions where there is a high prevalence of this deficien- 90 countries, putting nearly 3.3 billion people at risk of cy, further hampering transmission control efforts for this disease (Guerra et al. 2010, WHO 2012a). The prevalence parasite species (White 2008, Baird & Surjadjaja 2011). of G6PDd across countries was found to have a good cor- Despite the clinical and epidemiological significance of relation with those where, historically, malaria transmis- the interaction between G6PDd and malaria, the preva- sion has occurred (Howes et al. 2012). The explanation lence of G6PDd and the extent of its clinical consequences for this association has been that G6PDd is associated have not been properly measured in LA populations. with protection against P. falciparum (Mockenhaupt et al. In Brazil and other LA countries facing malaria as 2003, Clark et al. 2009) and P. vivax infections (Leslie a public health problem, the treatment recommendation et al. 2010, Santana et al. 2013). The mechanism confer- for P. vivax includes a full-course of PQ with no rou- ring resistance in G6PDd subjects may be related to an tine G6PDd screening. This short-sighted policy leads impaired antioxidant defence in ring-stage parasitised red to the prescription of potentially haemolytic drugs, put- cells, which could lead to membrane damage, triggering ting G6PDd individuals at risk of serious complications increased removal of infected cells by phagocytosis before (Lacerda et al. 2012b, Monteiro et al. 2014). We therefore parasite maturation to the trophozoite and schizont stages reviewed the existing literature to estimate the preva- (Ruwende et al. 1995). G6PDd is also thought to be a pro- lence of G6PDd in LA and to identify the most frequent tection factor against severe manifestations of malaria, al- variants that affect this population, highlighting areas though studies regarding which individuals, hemizygous where more research is necessary in the region. males or heterozygous females, may be protected present MATERIALS AND METHODS discrepancies (Ruwende et al. 1995, Guindo et al. 2007). In a context where the international community has A systematic review was performed to analyse the committed to a renewed malaria eradication agenda available published data on G6PDd prevalence, pheno- (malERA 2011), many countries have been planning to types and mutations in LA and the Caribbean. A broad reduce transmission or eliminate malaria, making the free text search was made using a previously published development and deployment of cost-effective strategies search strategy (Monteiro et al. 2014). Potentially relevant extremely necessary (Das & Horton 2010). Primaquine papers in all languages were accessed from MEDLINE (PQ), an 8-aminoquinoline, is currently the only Food and LILACS for a review of the full texts. Additional ar- and Drug Administration approved drug recommended ticles were obtained through citation tracking of reviews/ to treat hepatic stages of the P. vivax. The WHO rec- opinion articles and original papers. To identify relevant ommends that PQ should be used in radical cure for P. papers, two independent reviewers examined titles, ab- vivax malaria
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