Plasmodium falciparum Pfs47 haplotype compatibility to Anopheles gambiae in Kisumu, a malaria-endemic region of Kenya

Abstract Insecticide resistance and outdoor transmission have reduced the effectiveness of existing malaria transmission prevention strategies. As a result, targeted approaches to support continuing malaria control, such as transmission-blocking vaccines, are required. Cross-sectional mass blood scr...

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Main Authors: Shirley A. Onyango, Maxwell G. Machani, Kevin O. Ochwedo, Robin M. Oriango, Ming-Chieh Lee, Elizabeth Kokwaro, Yaw A. Afrane, Andrew K. Githeko, Daibin Zhong, Guiyun Yan
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Language:English
Published: Nature Portfolio 2025-02-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-84847-6
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author Shirley A. Onyango
Maxwell G. Machani
Kevin O. Ochwedo
Robin M. Oriango
Ming-Chieh Lee
Elizabeth Kokwaro
Yaw A. Afrane
Andrew K. Githeko
Daibin Zhong
Guiyun Yan
author_facet Shirley A. Onyango
Maxwell G. Machani
Kevin O. Ochwedo
Robin M. Oriango
Ming-Chieh Lee
Elizabeth Kokwaro
Yaw A. Afrane
Andrew K. Githeko
Daibin Zhong
Guiyun Yan
author_sort Shirley A. Onyango
collection DOAJ
description Abstract Insecticide resistance and outdoor transmission have reduced the effectiveness of existing malaria transmission prevention strategies. As a result, targeted approaches to support continuing malaria control, such as transmission-blocking vaccines, are required. Cross-sectional mass blood screening in children between 5 and 15 years was conducted in Chulaimbo, Kisumu, during the dry and wet seasons in 2018 and 2019. Plasmodium falciparum gametocyte carriers were identified by Microscopy. Subsequently, carriers were used to feed colony bred Anopheles gambiae females in serum replacement and whole blood membrane feeding experiments. The infection prevalence was 19.7% (95% Cl 0.003–0.007) with 95% of the infections being caused by P. falciparum. Of all confirmed P. falciparum infections, 16.9% were gametocytes. Thirty-seven paired experiments showed infection rates of 0.9% and 0.5% in the serum replacement and whole blood experiments, respectively, with no significant difference (P = 0.738). Six Pfs47 haplotypes were identified from 24 sequenced infectious blood samples: Hap_1 (E27D and L240I), Hap_2 (S98T); Hap_3 (E27D); Hap_4 (L240I); Hap_5 (E188D); and Hap_6 without mutations. Haplotype 4 had the highest frequency of 29.2% followed by Hap_3 and Hap_6 at 20.8% each then Hap_1 with a frequency of 16.7%, whereas Hap_5 and Hap_2 had frequencies of 8.3% and 4.2% respectively. Varying frequencies of Pfs47 haplotypes observed from genetically heterogeneous parasite populations in endemic regions illuminates vector compatibility to refracting P. falciparum using the hypothesized lock and key analogy. This acts as a bottleneck that increases the frequency of P. falciparum haplotypes that escape elimination by vector immune responses. The interaction can be used as a potential target for transmission blocking through a refractory host.
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spelling doaj-art-7e03e43b28eb49fe9649ec6a060a85b82025-08-20T02:59:32ZengNature PortfolioScientific Reports2045-23222025-02-011511810.1038/s41598-024-84847-6Plasmodium falciparum Pfs47 haplotype compatibility to Anopheles gambiae in Kisumu, a malaria-endemic region of KenyaShirley A. Onyango0Maxwell G. Machani1Kevin O. Ochwedo2Robin M. Oriango3Ming-Chieh Lee4Elizabeth Kokwaro5Yaw A. Afrane6Andrew K. Githeko7Daibin Zhong8Guiyun Yan9School of Zoological Sciences, Kenyatta UniversityCentre for Global Health Research, Kenya Medical Research InstituteInternational Centre of Excellence for Malaria Research, Tom Mboya UniversityInternational Centre of Excellence for Malaria Research, Tom Mboya UniversityProgram in Public Health, College of Health Sciences, University of California at IrvineSchool of Zoological Sciences, Kenyatta UniversityDepartment of Medical Microbiology, Medical School, University of GhanaCentre for Global Health Research, Kenya Medical Research InstituteProgram in Public Health, College of Health Sciences, University of California at IrvineProgram in Public Health, College of Health Sciences, University of California at IrvineAbstract Insecticide resistance and outdoor transmission have reduced the effectiveness of existing malaria transmission prevention strategies. As a result, targeted approaches to support continuing malaria control, such as transmission-blocking vaccines, are required. Cross-sectional mass blood screening in children between 5 and 15 years was conducted in Chulaimbo, Kisumu, during the dry and wet seasons in 2018 and 2019. Plasmodium falciparum gametocyte carriers were identified by Microscopy. Subsequently, carriers were used to feed colony bred Anopheles gambiae females in serum replacement and whole blood membrane feeding experiments. The infection prevalence was 19.7% (95% Cl 0.003–0.007) with 95% of the infections being caused by P. falciparum. Of all confirmed P. falciparum infections, 16.9% were gametocytes. Thirty-seven paired experiments showed infection rates of 0.9% and 0.5% in the serum replacement and whole blood experiments, respectively, with no significant difference (P = 0.738). Six Pfs47 haplotypes were identified from 24 sequenced infectious blood samples: Hap_1 (E27D and L240I), Hap_2 (S98T); Hap_3 (E27D); Hap_4 (L240I); Hap_5 (E188D); and Hap_6 without mutations. Haplotype 4 had the highest frequency of 29.2% followed by Hap_3 and Hap_6 at 20.8% each then Hap_1 with a frequency of 16.7%, whereas Hap_5 and Hap_2 had frequencies of 8.3% and 4.2% respectively. Varying frequencies of Pfs47 haplotypes observed from genetically heterogeneous parasite populations in endemic regions illuminates vector compatibility to refracting P. falciparum using the hypothesized lock and key analogy. This acts as a bottleneck that increases the frequency of P. falciparum haplotypes that escape elimination by vector immune responses. The interaction can be used as a potential target for transmission blocking through a refractory host.https://doi.org/10.1038/s41598-024-84847-6P. falciparumPfs47An. gambiaeCompatibilityGeographic regions
spellingShingle Shirley A. Onyango
Maxwell G. Machani
Kevin O. Ochwedo
Robin M. Oriango
Ming-Chieh Lee
Elizabeth Kokwaro
Yaw A. Afrane
Andrew K. Githeko
Daibin Zhong
Guiyun Yan
Plasmodium falciparum Pfs47 haplotype compatibility to Anopheles gambiae in Kisumu, a malaria-endemic region of Kenya
Scientific Reports
P. falciparum
Pfs47
An. gambiae
Compatibility
Geographic regions
title Plasmodium falciparum Pfs47 haplotype compatibility to Anopheles gambiae in Kisumu, a malaria-endemic region of Kenya
title_full Plasmodium falciparum Pfs47 haplotype compatibility to Anopheles gambiae in Kisumu, a malaria-endemic region of Kenya
title_fullStr Plasmodium falciparum Pfs47 haplotype compatibility to Anopheles gambiae in Kisumu, a malaria-endemic region of Kenya
title_full_unstemmed Plasmodium falciparum Pfs47 haplotype compatibility to Anopheles gambiae in Kisumu, a malaria-endemic region of Kenya
title_short Plasmodium falciparum Pfs47 haplotype compatibility to Anopheles gambiae in Kisumu, a malaria-endemic region of Kenya
title_sort plasmodium falciparum pfs47 haplotype compatibility to anopheles gambiae in kisumu a malaria endemic region of kenya
topic P. falciparum
Pfs47
An. gambiae
Compatibility
Geographic regions
url https://doi.org/10.1038/s41598-024-84847-6
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