Heterogeneity in prevalence of subclinical Plasmodium falciparum and Plasmodium vivax infections but no parasite genomic clustering in the Chittagong Hill Tracts, Bangladesh

Tiffany Huwe; Mohammad Golam Kibria; Fatema Tuj Johora; Ching Swe Phru; Nusrat Jahan; Mohammad Sharif Hossain; Wasif Ali Khan; Ric N. Price; Benedikt Ley; Mohammad Shafiul Alam; Cristian Koepfli

doi:10.1186/s12936-022-04236-0

Heterogeneity in prevalence of subclinical Plasmodium falciparum and Plasmodium vivax infections but no parasite genomic clustering in the Chittagong Hill Tracts, Bangladesh

Tiffany Huwe, Mohammad Golam Kibria, Fatema Tuj Johora, Ching Swe Phru, Nusrat Jahan, Mohammad Sharif Hossain, Wasif Ali Khan, Ric N. Price, Benedikt Ley, Mohammad Shafiul Alam, Cristian Koepfli

Global and Tropical Health

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Abstract

Background: Malaria remains endemic in Bangladesh, with the majority of cases occurring in forested, mountainous region in the Chittagong Hill Tracts (CHT). This area is home to Bengali and diverse groups of indigenous people (Pahari) residing largely in mono-ethnic villages.

Methods: 1002 individuals of the 9 most prominent Pahari and the Bengali population were randomly selected and screened by RDT and qPCR. Parasites were genotyped by msp2 and deep sequencing of 5 amplicons (ama1-D3, cpmp, cpp, csp, and msp7) for Plasmodium falciparum (n = 20), and by microsatellite (MS) typing of ten loci and amplicon sequencing of msp1 for Plasmodium vivax (n = 21). Population structure was analysed using STRUCTURE software. Identity-by-state (IBS) was calculated as a measure of parasite relatedness and used to generate relatedness networks.

Results: The prevalence of P. falciparum and P. vivax infection was 0.7% by RDT (P. falciparum 6/1002; P. vivax 0/1002, mixed: 1/1002) and 4% by qPCR (P. falciparum 21/1002; P. vivax 16/1002, mixed: 5/1002). Infections were highly clustered, with 64% (27/42) of infections occurring in only two Pahari groups, the Khumi and Mro. Diversity was high; expected heterozygosity was 0.93 for P. falciparum and 0.81 for P. vivax. 85.7% (18/21) of P. vivax and 25% (5/20) of P. falciparum infections were polyclonal. No population structure was evident for either species, suggesting high transmission and gene flow among Pahari groups.

Conclusions: High subclinical infection prevalence and genetic diversity mirror ongoing transmission. Control activities should be specifically directed to Pahari groups at greatest risk.

Original language	English
Article number	218
Pages (from-to)	1-11
Number of pages	11
Journal	Malaria Journal
Volume	21
Issue number	1
DOIs	https://doi.org/10.1186/s12936-022-04236-0
Publication status	Published - Dec 2022

Bibliographical note

Funding Information:
This project was supported, in part, by the Indiana Clinical and Translational Sciences Institute, funded, in part by Grant Number UL1TR002529 from the National Institutes of Health, National Center for Advancing Translational Sciences, Clinical and Translational Sciences Award; by NIH Grant R21AI137891, the Bill and Melinda Gates Foundation (OPP1054404 and OPP1164105), and the Eck Institute for Global Health at the University of Notre Dame. BL is funded by the Australian Department of Foreign Affairs and Trade. RNP is funded by the Wellcome Trust (Senior Fellowship in Clinical Science, 200909). icddr,b is grateful to the Governments of Bangladesh, Canada, Sweden and the UK for providing core/unrestricted support. No funding bodies had any role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Publisher Copyright:
© 2022, The Author(s).

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Huwe, T., Kibria, M. G., Johora, F. T., Phru, C. S., Jahan, N., Hossain, M. S., Khan, W. A., Price, R. N., Ley, B., Alam, M. S., & Koepfli, C. (2022). Heterogeneity in prevalence of subclinical Plasmodium falciparum and Plasmodium vivax infections but no parasite genomic clustering in the Chittagong Hill Tracts, Bangladesh. Malaria Journal, 21(1), 1-11. Article 218. https://doi.org/10.1186/s12936-022-04236-0

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title = "Heterogeneity in prevalence of subclinical Plasmodium falciparum and Plasmodium vivax infections but no parasite genomic clustering in the Chittagong Hill Tracts, Bangladesh",

abstract = "Background: Malaria remains endemic in Bangladesh, with the majority of cases occurring in forested, mountainous region in the Chittagong Hill Tracts (CHT). This area is home to Bengali and diverse groups of indigenous people (Pahari) residing largely in mono-ethnic villages. Methods: 1002 individuals of the 9 most prominent Pahari and the Bengali population were randomly selected and screened by RDT and qPCR. Parasites were genotyped by msp2 and deep sequencing of 5 amplicons (ama1-D3, cpmp, cpp, csp, and msp7) for Plasmodium falciparum (n = 20), and by microsatellite (MS) typing of ten loci and amplicon sequencing of msp1 for Plasmodium vivax (n = 21). Population structure was analysed using STRUCTURE software. Identity-by-state (IBS) was calculated as a measure of parasite relatedness and used to generate relatedness networks. Results: The prevalence of P. falciparum and P. vivax infection was 0.7% by RDT (P. falciparum 6/1002; P. vivax 0/1002, mixed: 1/1002) and 4% by qPCR (P. falciparum 21/1002; P. vivax 16/1002, mixed: 5/1002). Infections were highly clustered, with 64% (27/42) of infections occurring in only two Pahari groups, the Khumi and Mro. Diversity was high; expected heterozygosity was 0.93 for P. falciparum and 0.81 for P. vivax. 85.7% (18/21) of P. vivax and 25% (5/20) of P. falciparum infections were polyclonal. No population structure was evident for either species, suggesting high transmission and gene flow among Pahari groups. Conclusions: High subclinical infection prevalence and genetic diversity mirror ongoing transmission. Control activities should be specifically directed to Pahari groups at greatest risk.",

keywords = "Bangladesh, Chittagong Hill Tracts, Clustering, Ethnic groups, Genotyping, Malaria, Pahari, Plasmodium falciparum, Plasmodium vivax, Population structure",

author = "Tiffany Huwe and Kibria, {Mohammad Golam} and Johora, {Fatema Tuj} and Phru, {Ching Swe} and Nusrat Jahan and Hossain, {Mohammad Sharif} and Khan, {Wasif Ali} and Price, {Ric N.} and Benedikt Ley and Alam, {Mohammad Shafiul} and Cristian Koepfli",

note = "Funding Information: This project was supported, in part, by the Indiana Clinical and Translational Sciences Institute, funded, in part by Grant Number UL1TR002529 from the National Institutes of Health, National Center for Advancing Translational Sciences, Clinical and Translational Sciences Award; by NIH Grant R21AI137891, the Bill and Melinda Gates Foundation (OPP1054404 and OPP1164105), and the Eck Institute for Global Health at the University of Notre Dame. BL is funded by the Australian Department of Foreign Affairs and Trade. RNP is funded by the Wellcome Trust (Senior Fellowship in Clinical Science, 200909). icddr,b is grateful to the Governments of Bangladesh, Canada, Sweden and the UK for providing core/unrestricted support. No funding bodies had any role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1186/s12936-022-04236-0",

language = "English",

volume = "21",

pages = "1--11",

journal = "Malaria Journal",

issn = "1475-2875",

publisher = "BioMed Central",

number = "1",

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Huwe, T, Kibria, MG, Johora, FT, Phru, CS, Jahan, N, Hossain, MS, Khan, WA, Price, RN , Ley, B, Alam, MS & Koepfli, C 2022, 'Heterogeneity in prevalence of subclinical Plasmodium falciparum and Plasmodium vivax infections but no parasite genomic clustering in the Chittagong Hill Tracts, Bangladesh', Malaria Journal, vol. 21, no. 1, 218, pp. 1-11. https://doi.org/10.1186/s12936-022-04236-0

TY - JOUR

T1 - Heterogeneity in prevalence of subclinical Plasmodium falciparum and Plasmodium vivax infections but no parasite genomic clustering in the Chittagong Hill Tracts, Bangladesh

AU - Huwe, Tiffany

AU - Kibria, Mohammad Golam

AU - Johora, Fatema Tuj

AU - Phru, Ching Swe

AU - Jahan, Nusrat

AU - Hossain, Mohammad Sharif

AU - Khan, Wasif Ali

AU - Price, Ric N.

AU - Ley, Benedikt

AU - Alam, Mohammad Shafiul

AU - Koepfli, Cristian

N1 - Funding Information: This project was supported, in part, by the Indiana Clinical and Translational Sciences Institute, funded, in part by Grant Number UL1TR002529 from the National Institutes of Health, National Center for Advancing Translational Sciences, Clinical and Translational Sciences Award; by NIH Grant R21AI137891, the Bill and Melinda Gates Foundation (OPP1054404 and OPP1164105), and the Eck Institute for Global Health at the University of Notre Dame. BL is funded by the Australian Department of Foreign Affairs and Trade. RNP is funded by the Wellcome Trust (Senior Fellowship in Clinical Science, 200909). icddr,b is grateful to the Governments of Bangladesh, Canada, Sweden and the UK for providing core/unrestricted support. No funding bodies had any role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - Background: Malaria remains endemic in Bangladesh, with the majority of cases occurring in forested, mountainous region in the Chittagong Hill Tracts (CHT). This area is home to Bengali and diverse groups of indigenous people (Pahari) residing largely in mono-ethnic villages. Methods: 1002 individuals of the 9 most prominent Pahari and the Bengali population were randomly selected and screened by RDT and qPCR. Parasites were genotyped by msp2 and deep sequencing of 5 amplicons (ama1-D3, cpmp, cpp, csp, and msp7) for Plasmodium falciparum (n = 20), and by microsatellite (MS) typing of ten loci and amplicon sequencing of msp1 for Plasmodium vivax (n = 21). Population structure was analysed using STRUCTURE software. Identity-by-state (IBS) was calculated as a measure of parasite relatedness and used to generate relatedness networks. Results: The prevalence of P. falciparum and P. vivax infection was 0.7% by RDT (P. falciparum 6/1002; P. vivax 0/1002, mixed: 1/1002) and 4% by qPCR (P. falciparum 21/1002; P. vivax 16/1002, mixed: 5/1002). Infections were highly clustered, with 64% (27/42) of infections occurring in only two Pahari groups, the Khumi and Mro. Diversity was high; expected heterozygosity was 0.93 for P. falciparum and 0.81 for P. vivax. 85.7% (18/21) of P. vivax and 25% (5/20) of P. falciparum infections were polyclonal. No population structure was evident for either species, suggesting high transmission and gene flow among Pahari groups. Conclusions: High subclinical infection prevalence and genetic diversity mirror ongoing transmission. Control activities should be specifically directed to Pahari groups at greatest risk.

AB - Background: Malaria remains endemic in Bangladesh, with the majority of cases occurring in forested, mountainous region in the Chittagong Hill Tracts (CHT). This area is home to Bengali and diverse groups of indigenous people (Pahari) residing largely in mono-ethnic villages. Methods: 1002 individuals of the 9 most prominent Pahari and the Bengali population were randomly selected and screened by RDT and qPCR. Parasites were genotyped by msp2 and deep sequencing of 5 amplicons (ama1-D3, cpmp, cpp, csp, and msp7) for Plasmodium falciparum (n = 20), and by microsatellite (MS) typing of ten loci and amplicon sequencing of msp1 for Plasmodium vivax (n = 21). Population structure was analysed using STRUCTURE software. Identity-by-state (IBS) was calculated as a measure of parasite relatedness and used to generate relatedness networks. Results: The prevalence of P. falciparum and P. vivax infection was 0.7% by RDT (P. falciparum 6/1002; P. vivax 0/1002, mixed: 1/1002) and 4% by qPCR (P. falciparum 21/1002; P. vivax 16/1002, mixed: 5/1002). Infections were highly clustered, with 64% (27/42) of infections occurring in only two Pahari groups, the Khumi and Mro. Diversity was high; expected heterozygosity was 0.93 for P. falciparum and 0.81 for P. vivax. 85.7% (18/21) of P. vivax and 25% (5/20) of P. falciparum infections were polyclonal. No population structure was evident for either species, suggesting high transmission and gene flow among Pahari groups. Conclusions: High subclinical infection prevalence and genetic diversity mirror ongoing transmission. Control activities should be specifically directed to Pahari groups at greatest risk.

KW - Bangladesh

KW - Chittagong Hill Tracts

KW - Clustering

KW - Ethnic groups

KW - Genotyping

KW - Malaria

KW - Pahari

KW - Plasmodium falciparum

KW - Plasmodium vivax

KW - Population structure

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U2 - 10.1186/s12936-022-04236-0

DO - 10.1186/s12936-022-04236-0

M3 - Article

C2 - 35836171

AN - SCOPUS:85134139467

SN - 1475-2875

VL - 21

SP - 1

EP - 11

JO - Malaria Journal

JF - Malaria Journal

IS - 1

M1 - 218

ER -

Heterogeneity in prevalence of subclinical Plasmodium falciparum and Plasmodium vivax infections but no parasite genomic clustering in the Chittagong Hill Tracts, Bangladesh

Abstract

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