Impact of piperaquine resistance in Plasmodium falciparum on malaria treatment effectiveness in The Guianas: a descriptive epidemiological study - 25/01/24

Doi : 10.1016/S1473-3099(23)00502-9

Celia Florimond, PhD ^a, Franck de Laval, MD ^b,^c, Angela M Early, PhD ^d,^e, Swaélie Sauthier, MSc ^a, Yassamine Lazrek, PhD ^a, Stéphane Pelleau, PhD ^a,^f, Wuelton M Monteiro, PhD ^g,^h, Maxime Agranier, PharmD ^a, Nicolas Taudon, PharmD ⁱ, François Morin, MD ^b, Magda Magris, PhD ^j, Marcus V G Lacerda, MD ^g,^k, Giselle M R Viana, PhD ^l, Sócrates Herrera, MD ^m,ⁿ, Malti R Adhin, PhD ^o, Marcelo U Ferreira, ProfMD ^p,^q, Charles J Woodrow, PhD ^r,^s, Ghulam R Awab, ProfMD ^r,^t, Horace Cox, MD ^u, Maria-Paz Ade, MSc ^v, Emilie Mosnier, MD ^c, Félix Djossou, ProfMD ^w, Daniel E Neafsey, PhD ^d,^e, Pascal Ringwald, MD ^x, Lise Musset, PharmD ^a,⁎

^a Laboratoire de parasitologie, World Health Organization Collaborating Center for Surveillance of Antimalarial Drug Resistance, Center Nationale de Référence du Paludisme, Institut Pasteur de la Guyane, Cayenne, French Guiana

^b Service de Santé des Armées (SSA), Centre d’Epidémiologie et de Santé Publique des Armées (CESPA), Marseille, France

^c Sciences Economiques Sociales de la Santé & Traitement de l’Information Médicale (SESSTIM), Aix Marseille University, INSERM, IRD, Marseille, France

^d Infectious Disease and Microbiome Program, Broad Institute, Cambridge, MA, USA

^e Department of Immunology and Infectious Diseases, Harvard T H Chan School of Public Health, Boston, MA, USA

^f Infectious Diseases Epidemiology and Analytics Unit, Department of Global Health, Institut Pasteur, Université Paris Cité, Paris, France

^g Diretoria de Ensino e Pesquisa, Fundação de Medicina Tropical Dr Heitor Vieira Dourado, Manaus, Brazil

^h Escola de Ciências da Saúde, Universidade do Estado do Amazonas, Manaus, Brazil

ⁱ Unité de développements analytiques et bioanalyse, Institut de recherche biomédicale des armées, Brétigny-sur-Orge, France

^j Amazonic Center for Research and Control of Tropical Diseases “Simón Bolívar”, Puerto Ayacucho, Venezuela

^k Instituto Leônidas & Maria Deane, Fiocruz, Manaus, Brazil

^l Laboratory of Basic Research in Malaria, Evandro Chagas Institute, Brazil Ministry of Health, Ananindeua, Brazil

^m Malaria Vaccine and Drug Development Center, Cali, Colombia

ⁿ Caucaseco Scientific Research Center, Cali, Colombia

^o Department of Biochemistry Kernkampweg 5, Faculty of Medical Sciences, Anton de Kom Universiteit van Suriname, Paramaribo, Suriname

^p Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil

^q Global Health and Tropical Medicine, Institute of Hygiene and Tropical Medicine, Nova University of Lisbon, Lisbon, Portugal

^r Mahidol Oxford Tropical Medicine Research Unit (MORU), Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand

^s Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, UK

^t Ministry of Public Health, Kabul, Afghanistan

^u National Malaria Program, Ministry of Health, Georgetown, Guyana

^v Department of Communicable Diseases and Environmental Determinants of Health, Pan American Health Organization/World Health Organization, Washington DC, USA

^w Infectious and Tropical Diseases Unit, Cayenne General Hospital, Cayenne, French Guiana

^x Global Malaria Programme, World Health Organization, Geneva, Switzerland

^* Correspondence to: Dr L Musset, Laboratoire de parasitologie, World Health Organization Collaborating Center for Surveillance of Antimalarial Drug Resistance, Center Nationale de Référence du Paludisme, Institut Pasteur de la Guyane, Cayenne 97306, French Guiana Laboratoire de parasitologie World Health Organization Collaborating Center for Surveillance of Antimalarial Drug Resistance Center Nationale de Référence du Paludisme Institut Pasteur de la Guyane Cayenne 97306 French Guiana

Summary

Background

Plasmodium falciparum is an apicomplexan parasite responsible for lethal cases of malaria. According to WHO recommendations, P falciparum cases are treated with artemisinin-based combination therapy including dihydroartemisinin–piperaquine. However, the emergence of resistant parasites against dihydroartemisinin–piperaquine was reported in southeast Asia in 2008 and, a few years later, suspected in South America.

Methods

To characterise resistance emergence, a treatment efficacy study was performed on the reported patients infected with P falciparum and treated with dihydroartemisinin–piperaquine in French Guiana (n=6, 2016–18). Contemporary isolates collected in French Guiana were genotyped for P falciparum chloroquine resistance transporter (pfCRT; n=845) and pfpm2 and pfpm3 copy number (n=231), phenotyped using the in vitro piperaquine survival assay (n=86), and analysed through genomic studies (n=50). Additional samples from five Amazonian countries and one outside the region were genotyped (n=1440).

Findings

In field isolates, 40 (47%) of 86 (95% CI 35·9–57·1) were resistant to piperaquine in vitro; these phenotypes were more associated with pfCRT^C350R (ie, Cys350Arg) and pfpm2 and pfpm3 amplifications (Dunn test, p<0·001). Those markers were also associated with dihydroartemisinin–piperaquine treatment failure (n=3 [50%] of 6). A high prevalence of piperaquine resistance markers was observed in Suriname in 19 (83%) of 35 isolates and in Guyana in 579 (73%) of 791 isolates. The pfCRT^C350R mutation emerged before pfpm2 and pfpm3 amplification in a temporal sequence different from southeast Asia, and in the absence of artemisinin partial resistance, suggesting a geographically distinctive epistatic relationship between these genetic markers.

Interpretation

The high prevalence of piperaquine resistance markers in parasite populations of the Guianas, and the risk of associated therapeutic failures calls for caution on dihydroartemisinin–piperaquine use in the region. Furthermore, greater attention should be given to potential differences in genotype to phenotype mapping across genetically distinct parasite populations from different continents.

Funding

Pan American Health Organization and WHO, French Ministry for Research, European Commission, Santé publique France, Agence Nationale de la Recherche, Fundação de Amparo à Pesquisa do Estado do Amazonas, Ministry of Health of Brazil, Oswaldo Cruz Foundation, and National Institutes of Health.

Translations

For the French and Portuguese translations of the abstract see Supplementary Materials section.

Le texte complet de cet article est disponible en PDF.

Plan

Genotyping and genomic analysis

In vitro drug sensitivity assays (ring-stage survival assay)

Statistical analysis

Role of the funding source

Results

Discussion

Data sharing

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Vol 24 - N° 2

P. 161-171 - février 2024 Retour au numéro

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Impact of piperaquine resistance in Plasmodium falciparum on malaria treatment effectiveness in The Guianas: a descriptive epidemiological study - 25/01/24

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