Plasmodium vivax genomic surveillance in the Peruvian Amazon with Pv AmpliSeq assay.


Journal

PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488

Informations de publication

Date de publication:
11 Jul 2024
Historique:
received: 21 12 2023
accepted: 12 06 2024
medline: 11 7 2024
pubmed: 11 7 2024
entrez: 11 7 2024
Statut: aheadofprint

Résumé

Plasmodium vivax is the most predominant malaria species in Latin America, constituting 71.5% of malaria cases in 2021. With several countries aiming for malaria elimination, it is crucial to prioritize effectiveness of national control programs by optimizing the utilization of available resources and strategically implementing necessary changes. To support this, there is a need for innovative approaches such as genomic surveillance tools that can investigate changes in transmission intensity, imported cases and sources of reintroduction, and can detect molecular markers associated with drug resistance. Here, we apply a modified highly-multiplexed deep sequencing assay: Pv AmpliSeq v2 Peru. The tool targets a newly developed 41-SNP Peru barcode for parasite population analysis within Peru, the 33-SNP vivaxGEN-geo panel for country-level classification, and 11 putative drug resistance genes. It was applied to 230 samples from the Peruvian Amazon (2007-2020), generating baseline surveillance data. We observed a heterogenous P. vivax population with high diversity and gene flow in peri-urban areas of Maynas province (Loreto region) with a temporal drift using all SNPs detected by the assay (nSNP = 2909). In comparison, in an indigenous isolated area, the parasite population was genetically differentiated (FST = 0.07-0.09) with moderate diversity and high relatedness between isolates in the community. In a remote border community, a clonal P. vivax cluster was identified, with distinct haplotypes in drug resistant genes and ama1, more similar to Brazilian isolates, likely representing an introduction of P. vivax from Brazil at that time. To test its applicability for Latin America, we evaluated the SNP Peru barcode in P. vivax genomes from the region and demonstrated the capacity to capture local population clustering at within-country level. Together this data shows that P. vivax transmission is heterogeneous in different settings within the Peruvian Amazon. Genetic analysis is a key component for regional malaria control, offering valuable insights that should be incorporated into routine surveillance.

Sections du résumé

BACKGROUND BACKGROUND
Plasmodium vivax is the most predominant malaria species in Latin America, constituting 71.5% of malaria cases in 2021. With several countries aiming for malaria elimination, it is crucial to prioritize effectiveness of national control programs by optimizing the utilization of available resources and strategically implementing necessary changes. To support this, there is a need for innovative approaches such as genomic surveillance tools that can investigate changes in transmission intensity, imported cases and sources of reintroduction, and can detect molecular markers associated with drug resistance.
METHODOLOGY/PRINCIPAL FINDINGS RESULTS
Here, we apply a modified highly-multiplexed deep sequencing assay: Pv AmpliSeq v2 Peru. The tool targets a newly developed 41-SNP Peru barcode for parasite population analysis within Peru, the 33-SNP vivaxGEN-geo panel for country-level classification, and 11 putative drug resistance genes. It was applied to 230 samples from the Peruvian Amazon (2007-2020), generating baseline surveillance data. We observed a heterogenous P. vivax population with high diversity and gene flow in peri-urban areas of Maynas province (Loreto region) with a temporal drift using all SNPs detected by the assay (nSNP = 2909). In comparison, in an indigenous isolated area, the parasite population was genetically differentiated (FST = 0.07-0.09) with moderate diversity and high relatedness between isolates in the community. In a remote border community, a clonal P. vivax cluster was identified, with distinct haplotypes in drug resistant genes and ama1, more similar to Brazilian isolates, likely representing an introduction of P. vivax from Brazil at that time. To test its applicability for Latin America, we evaluated the SNP Peru barcode in P. vivax genomes from the region and demonstrated the capacity to capture local population clustering at within-country level.
CONCLUSIONS/SIGNIFICANCE CONCLUSIONS
Together this data shows that P. vivax transmission is heterogeneous in different settings within the Peruvian Amazon. Genetic analysis is a key component for regional malaria control, offering valuable insights that should be incorporated into routine surveillance.

Identifiants

pubmed: 38991038
doi: 10.1371/journal.pntd.0011879
pii: PNTD-D-23-01634
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0011879

Informations de copyright

Copyright: © 2024 Kattenberg et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Auteurs

Johanna Helena Kattenberg (JH)

Malariology Unit, Biomedical Sciences Department, Institute of Tropical Medicine, Antwerp, Belgium.

Luis Cabrera-Sosa (L)

Instituto de Medicina Tropical "Alexander von Humboldt", Universidad Peruana Cayetano Heredia, Lima, Peru.
Laboratorio de Malaria: Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias e Ingeniería, Universidad Peruana Cayetano Heredia, Lima, Peru.
Malaria Research Group (MaRCH), Global Health Institute, Faculty of Medicine, University of Antwerp, Antwerp, Belgium.

Erick Figueroa-Ildefonso (E)

Instituto de Medicina Tropical "Alexander von Humboldt", Universidad Peruana Cayetano Heredia, Lima, Peru.
Laboratorio de Malaria: Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias e Ingeniería, Universidad Peruana Cayetano Heredia, Lima, Peru.

Mathijs Mutsaers (M)

Malariology Unit, Biomedical Sciences Department, Institute of Tropical Medicine, Antwerp, Belgium.

Pieter Monsieurs (P)

Malariology Unit, Biomedical Sciences Department, Institute of Tropical Medicine, Antwerp, Belgium.

Pieter Guetens (P)

Malariology Unit, Biomedical Sciences Department, Institute of Tropical Medicine, Antwerp, Belgium.

Berónica Infante (B)

Instituto de Medicina Tropical "Alexander von Humboldt", Universidad Peruana Cayetano Heredia, Lima, Peru.
Laboratorio de Malaria: Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias e Ingeniería, Universidad Peruana Cayetano Heredia, Lima, Peru.

Christopher Delgado-Ratto (C)

Malaria Research Group (MaRCH), Global Health Institute, Faculty of Medicine, University of Antwerp, Antwerp, Belgium.

Dionicia Gamboa (D)

Instituto de Medicina Tropical "Alexander von Humboldt", Universidad Peruana Cayetano Heredia, Lima, Peru.
Laboratorio de Malaria: Parásitos y Vectores, Laboratorios de Investigación y Desarrollo, Facultad de Ciencias e Ingeniería, Universidad Peruana Cayetano Heredia, Lima, Peru.
Departamento de Ciencias Celulares y Moleculares, Facultad de Ciencias e Ingeniería, Universidad Peruana Cayetano Heredia, Lima, Peru.

Anna Rosanas-Urgell (A)

Malariology Unit, Biomedical Sciences Department, Institute of Tropical Medicine, Antwerp, Belgium.

Classifications MeSH