Retrospective analysis of Plasmodium vivax genomes from a pre-elimination China inland population in the 2010s
IntroductionIn malaria-free countries, imported cases are challenging because interconnections with neighboring countries with higher transmission rates increase the risk of parasite reintroduction. Establishing a genetic database for rapidly identifying malaria importation or reintroduction is cruc...
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1071689/full |
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| author | Ying Liu Ying Liu Ying Liu Ying Liu Ying Liu Tao Zhang Shen-Bo Chen Shen-Bo Chen Shen-Bo Chen Shen-Bo Chen Yan-Bing Cui Yan-Bing Cui Yan-Bing Cui Yan-Bing Cui Shu-Qi Wang Hong-Wei Zhang Hai-Mo Shen Hai-Mo Shen Hai-Mo Shen Hai-Mo Shen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen |
| author_facet | Ying Liu Ying Liu Ying Liu Ying Liu Ying Liu Tao Zhang Shen-Bo Chen Shen-Bo Chen Shen-Bo Chen Shen-Bo Chen Yan-Bing Cui Yan-Bing Cui Yan-Bing Cui Yan-Bing Cui Shu-Qi Wang Hong-Wei Zhang Hai-Mo Shen Hai-Mo Shen Hai-Mo Shen Hai-Mo Shen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen |
| author_sort | Ying Liu |
| collection | DOAJ |
| description | IntroductionIn malaria-free countries, imported cases are challenging because interconnections with neighboring countries with higher transmission rates increase the risk of parasite reintroduction. Establishing a genetic database for rapidly identifying malaria importation or reintroduction is crucial in addressing these challenges. This study aimed to examine genomic epidemiology during the pre-elimination stage by retrospectively reporting whole-genome sequence variation of 10 Plasmodium vivax isolates from inland China.MethodsThe samples were collected during the last few inland outbreaks from 2011 to 2012 when China implemented a malaria control plan. After next-generation sequencing, we completed a genetic analysis of the population, explored the geographic specificity of the samples, and examined clustering of selection pressures. We also scanned genes for signals of positive selection.ResultsChina’s inland populations were highly structured compared to the surrounding area, with a single potential ancestor. Additionally, we identified genes under selection and evaluated the selection pressure on drug-resistance genes. In the inland population, positive selection was detected in some critical gene families, including sera, msp3, and vir. Meanwhile, we identified selection signatures in drug resistance, such as ugt, krs1, and crt, and noticed that the ratio of wild-type dhps and dhfr-ts increased after China banned sulfadoxine-pyrimethamine (SP) for decades.DiscussionOur data provides an opportunity to investigate the molecular epidemiology of pre-elimination inland malaria populations, which exhibited lower selection pressure on invasion and immune evasion genes than neighbouring areas, but increased drug resistance in low transmission settings. Our results revealed that the inland population was severely fragmented with low relatedness among infections, despite a higher incidence of multiclonal infections, suggesting that superinfection or co-transmission events are rare in low-endemic circumstances. We identified selective signatures of resistance and found that the proportion of susceptible isolates fluctuated in response to the prohibition of specific drugs. This finding is consistent with the alterations in medication strategies during the malaria elimination campaign in inland China. Such findings could provide a genetic basis for future population studies, assessing changes in other pre-elimination countries. |
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| spelling | doaj.art-7f9b35816b684c4f9773f33b7141f3c42023-02-09T12:07:21ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-02-011410.3389/fmicb.2023.10716891071689Retrospective analysis of Plasmodium vivax genomes from a pre-elimination China inland population in the 2010sYing Liu0Ying Liu1Ying Liu2Ying Liu3Ying Liu4Tao Zhang5Shen-Bo Chen6Shen-Bo Chen7Shen-Bo Chen8Shen-Bo Chen9Yan-Bing Cui10Yan-Bing Cui11Yan-Bing Cui12Yan-Bing Cui13Shu-Qi Wang14Hong-Wei Zhang15Hai-Mo Shen16Hai-Mo Shen17Hai-Mo Shen18Hai-Mo Shen19Jun-Hu Chen20Jun-Hu Chen21Jun-Hu Chen22Jun-Hu Chen23Jun-Hu Chen24National Institute of Parasitic Diseases, Chinese Center for Diseases Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai, ChinaNational Health Commission of the People’s Republic of China (NHC) Key Laboratory of Parasite and Vector Biology, Shanghai, ChinaWorld Health Organization (WHO) Collaborating Center for Tropical Diseases, Shanghai, ChinaNational Center for International Research on Tropical Diseases, Shanghai, ChinaHenan Provincial Center for Disease Control and Prevention, Zhengzhou, ChinaAnhui Provincial Center for Disease Control and Prevention, Hefei, ChinaNational Institute of Parasitic Diseases, Chinese Center for Diseases Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai, ChinaNational Health Commission of the People’s Republic of China (NHC) Key Laboratory of Parasite and Vector Biology, Shanghai, ChinaWorld Health Organization (WHO) Collaborating Center for Tropical Diseases, Shanghai, ChinaNational Center for International Research on Tropical Diseases, Shanghai, ChinaNational Institute of Parasitic Diseases, Chinese Center for Diseases Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai, ChinaNational Health Commission of the People’s Republic of China (NHC) Key Laboratory of Parasite and Vector Biology, Shanghai, ChinaWorld Health Organization (WHO) Collaborating Center for Tropical Diseases, Shanghai, ChinaNational Center for International Research on Tropical Diseases, Shanghai, ChinaAnhui Provincial Center for Disease Control and Prevention, Hefei, ChinaHenan Provincial Center for Disease Control and Prevention, Zhengzhou, ChinaNational Institute of Parasitic Diseases, Chinese Center for Diseases Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai, ChinaNational Health Commission of the People’s Republic of China (NHC) Key Laboratory of Parasite and Vector Biology, Shanghai, ChinaWorld Health Organization (WHO) Collaborating Center for Tropical Diseases, Shanghai, ChinaNational Center for International Research on Tropical Diseases, Shanghai, ChinaNational Institute of Parasitic Diseases, Chinese Center for Diseases Control and Prevention (Chinese Center for Tropical Diseases Research), Shanghai, ChinaNational Health Commission of the People’s Republic of China (NHC) Key Laboratory of Parasite and Vector Biology, Shanghai, ChinaWorld Health Organization (WHO) Collaborating Center for Tropical Diseases, Shanghai, ChinaNational Center for International Research on Tropical Diseases, Shanghai, ChinaSchool of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaIntroductionIn malaria-free countries, imported cases are challenging because interconnections with neighboring countries with higher transmission rates increase the risk of parasite reintroduction. Establishing a genetic database for rapidly identifying malaria importation or reintroduction is crucial in addressing these challenges. This study aimed to examine genomic epidemiology during the pre-elimination stage by retrospectively reporting whole-genome sequence variation of 10 Plasmodium vivax isolates from inland China.MethodsThe samples were collected during the last few inland outbreaks from 2011 to 2012 when China implemented a malaria control plan. After next-generation sequencing, we completed a genetic analysis of the population, explored the geographic specificity of the samples, and examined clustering of selection pressures. We also scanned genes for signals of positive selection.ResultsChina’s inland populations were highly structured compared to the surrounding area, with a single potential ancestor. Additionally, we identified genes under selection and evaluated the selection pressure on drug-resistance genes. In the inland population, positive selection was detected in some critical gene families, including sera, msp3, and vir. Meanwhile, we identified selection signatures in drug resistance, such as ugt, krs1, and crt, and noticed that the ratio of wild-type dhps and dhfr-ts increased after China banned sulfadoxine-pyrimethamine (SP) for decades.DiscussionOur data provides an opportunity to investigate the molecular epidemiology of pre-elimination inland malaria populations, which exhibited lower selection pressure on invasion and immune evasion genes than neighbouring areas, but increased drug resistance in low transmission settings. Our results revealed that the inland population was severely fragmented with low relatedness among infections, despite a higher incidence of multiclonal infections, suggesting that superinfection or co-transmission events are rare in low-endemic circumstances. We identified selective signatures of resistance and found that the proportion of susceptible isolates fluctuated in response to the prohibition of specific drugs. This finding is consistent with the alterations in medication strategies during the malaria elimination campaign in inland China. Such findings could provide a genetic basis for future population studies, assessing changes in other pre-elimination countries.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1071689/fullmalariaChina inlandPlasmodium vivaxhaplotype-based detectingpositive selectiondrug resistance |
| spellingShingle | Ying Liu Ying Liu Ying Liu Ying Liu Ying Liu Tao Zhang Shen-Bo Chen Shen-Bo Chen Shen-Bo Chen Shen-Bo Chen Yan-Bing Cui Yan-Bing Cui Yan-Bing Cui Yan-Bing Cui Shu-Qi Wang Hong-Wei Zhang Hai-Mo Shen Hai-Mo Shen Hai-Mo Shen Hai-Mo Shen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen Jun-Hu Chen Retrospective analysis of Plasmodium vivax genomes from a pre-elimination China inland population in the 2010s Frontiers in Microbiology malaria China inland Plasmodium vivax haplotype-based detecting positive selection drug resistance |
| title | Retrospective analysis of Plasmodium vivax genomes from a pre-elimination China inland population in the 2010s |
| title_full | Retrospective analysis of Plasmodium vivax genomes from a pre-elimination China inland population in the 2010s |
| title_fullStr | Retrospective analysis of Plasmodium vivax genomes from a pre-elimination China inland population in the 2010s |
| title_full_unstemmed | Retrospective analysis of Plasmodium vivax genomes from a pre-elimination China inland population in the 2010s |
| title_short | Retrospective analysis of Plasmodium vivax genomes from a pre-elimination China inland population in the 2010s |
| title_sort | retrospective analysis of plasmodium vivax genomes from a pre elimination china inland population in the 2010s |
| topic | malaria China inland Plasmodium vivax haplotype-based detecting positive selection drug resistance |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1071689/full |
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