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Multiplexed ddPCR-amplicon sequencing reveals isolated Plasmodium falciparum populations amenable to local elimination in Zanzibar, Tanzania

Author

Listed:
  • Aurel Holzschuh

    (University of Notre Dame
    Swiss Tropical and Public Health Institute)

  • Anita Lerch

    (University of Notre Dame)

  • Inna Gerlovina

    (University of California)

  • Bakar S. Fakih

    (Swiss Tropical and Public Health Institute
    University of Basel
    Ifakara Health Institute)

  • Abdul-wahid H. Al-mafazy

    (Research Triangle Institute (RTI) International)

  • Erik J. Reaves

    (U.S. Centers for Disease Control and Prevention, President’s Malaria Initiative)

  • Abdullah Ali

    (Zanzibar Malaria Elimination Programme)

  • Faiza Abbas

    (Zanzibar Malaria Elimination Programme)

  • Mohamed Haji Ali

    (Zanzibar Malaria Elimination Programme)

  • Mohamed Ali Ali

    (Zanzibar Malaria Elimination Programme)

  • Manuel W. Hetzel

    (Swiss Tropical and Public Health Institute
    University of Basel)

  • Joshua Yukich

    (Tulane University)

  • Cristian Koepfli

    (University of Notre Dame)

Abstract

Zanzibar has made significant progress toward malaria elimination, but recent stagnation requires novel approaches. We developed a highly multiplexed droplet digital PCR (ddPCR)-based amplicon sequencing method targeting 35 microhaplotypes and drug-resistance loci, and successfully sequenced 290 samples from five districts covering both main islands. Here, we elucidate fine-scale Plasmodium falciparum population structure and infer relatedness and connectivity of infections using an identity-by-descent (IBD) approach. Despite high genetic diversity, we observe pronounced fine-scale spatial and temporal parasite genetic structure. Clusters of near-clonal infections on Pemba indicate persistent local transmission with limited parasite importation, presenting an opportunity for local elimination efforts. Furthermore, we observe an admixed parasite population on Unguja and detect a substantial fraction (2.9%) of significantly related infection pairs between Zanzibar and the mainland, suggesting recent importation. Our study provides a high-resolution view of parasite genetic structure across the Zanzibar archipelago and provides actionable insights for prioritizing malaria elimination efforts.

Suggested Citation

  • Aurel Holzschuh & Anita Lerch & Inna Gerlovina & Bakar S. Fakih & Abdul-wahid H. Al-mafazy & Erik J. Reaves & Abdullah Ali & Faiza Abbas & Mohamed Haji Ali & Mohamed Ali Ali & Manuel W. Hetzel & Joshu, 2023. "Multiplexed ddPCR-amplicon sequencing reveals isolated Plasmodium falciparum populations amenable to local elimination in Zanzibar, Tanzania," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39417-1
    DOI: 10.1038/s41467-023-39417-1
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    References listed on IDEAS

    as
    1. Aatreyee M. Das & Manuel W. Hetzel & Joshua O. Yukich & Logan Stuck & Bakar S. Fakih & Abdul-wahid H. Al-mafazy & Abdullah Ali & Nakul Chitnis, 2023. "Modelling the impact of interventions on imported, introduced and indigenous malaria infections in Zanzibar, Tanzania," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Hannah C. Slater & Amanda Ross & Ingrid Felger & Natalie E. Hofmann & Leanne Robinson & Jackie Cook & Bronner P. Gonçalves & Anders Björkman & Andre Lin Ouedraogo & Ulrika Morris & Mwinyi Msellem & Cr, 2019. "The temporal dynamics and infectiousness of subpatent Plasmodium falciparum infections in relation to parasite density," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    3. Hannah C. Slater & Amanda Ross & Ingrid Felger & Natalie E. Hofmann & Leanne Robinson & Jackie Cook & Bronner P. Gonçalves & Anders Björkman & Andre Lin Ouedraogo & Ulrika Morris & Mwinyi Msellem & Cr, 2019. "Author Correction: The temporal dynamics and infectiousness of subpatent Plasmodium falciparum infections in relation to parasite density," Nature Communications, Nature, vol. 10(1), pages 1-2, December.
    4. Amol C. Shetty & Christopher G. Jacob & Fang Huang & Yao Li & Sonia Agrawal & David L. Saunders & Chanthap Lon & Mark M. Fukuda & Pascal Ringwald & Elizabeth A. Ashley & Kay Thwe Han & Tin Maung Hlain, 2019. "Genomic structure and diversity of Plasmodium falciparum in Southeast Asia reveal recent parasite migration patterns," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
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    6. Patrick K. Tumwebaze & Melissa D. Conrad & Martin Okitwi & Stephen Orena & Oswald Byaruhanga & Thomas Katairo & Jennifer Legac & Shreeya Garg & David Giesbrecht & Sawyer R. Smith & Frida G. Ceja & Sam, 2022. "Decreased susceptibility of Plasmodium falciparum to both dihydroartemisinin and lumefantrine in northern Uganda," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. M. Isabel Veiga & Satish K. Dhingra & Philipp P. Henrich & Judith Straimer & Nina Gnädig & Anne-Catrin Uhlemann & Rowena E. Martin & Adele M. Lehane & David A. Fidock, 2016. "Globally prevalent PfMDR1 mutations modulate Plasmodium falciparum susceptibility to artemisinin-based combination therapies," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
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