Influence of the sickle cell trait on Plasmodium falciparum infectivity from naturally infected gametocyte carriers
Abstract Background Sickle cell trait (SCT) refers to the carriage of one abnormal copy of the β-globin gene, the HbS allele. SCT offers protection against malaria, controlling parasite density and preventing progression to symptomatic malaria. However, it remains unclear whether SCT also affects tr...
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| Format: | Article |
| Language: | English |
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BMC
2023-05-01
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| Series: | BMC Infectious Diseases |
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| Online Access: | https://doi.org/10.1186/s12879-023-08134-x |
| _version_ | 1797827654781501440 |
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| author | Christelle M. Ngou Albert N. Bayibéki Luc Abate Olesula S. Makinde Lionel B. Feufack-Donfack Elangwe M. Sarah-Matio Aline G. Bouopda-Tuedom Paul Taconet Nicolas Moiroux Parfait H. Awono-Ambéné Arthur Talman Lawrence S. Ayong Antoine Berry Sandrine E. Nsango Isabelle Morlais |
| author_facet | Christelle M. Ngou Albert N. Bayibéki Luc Abate Olesula S. Makinde Lionel B. Feufack-Donfack Elangwe M. Sarah-Matio Aline G. Bouopda-Tuedom Paul Taconet Nicolas Moiroux Parfait H. Awono-Ambéné Arthur Talman Lawrence S. Ayong Antoine Berry Sandrine E. Nsango Isabelle Morlais |
| author_sort | Christelle M. Ngou |
| collection | DOAJ |
| description | Abstract Background Sickle cell trait (SCT) refers to the carriage of one abnormal copy of the β-globin gene, the HbS allele. SCT offers protection against malaria, controlling parasite density and preventing progression to symptomatic malaria. However, it remains unclear whether SCT also affects transmission stages and mosquito infection parameters. Deciphering the impact of the SCT on human to mosquito malaria transmission is key to understanding mechanisms that maintain the trait in malaria endemic areas. Methods The study was conducted from June to July 2017 among asymptomatic children living in the locality of Mfou, Cameroon. Blood samples were collected from asymptomatic children to perform malaria diagnosis by microscopy, Plasmodium species by PCR and hemoglobin typing by RFLP. Infectiousness of gametocytes to mosquitoes was assessed by membrane feeding assays using blood from gametocyte carriers of HbAA and HbAS genotypes. A zero-inflated model was fitted to predict distribution of oocysts in mosquitoes according to hemoglobin genotype of the gametocyte source. Results Among the 1557 children enrolled in the study, 314 (20.16%) were of the HbAS genotype. The prevalence of children with P. falciparum gametocytes was 18.47% in HbAS individuals and 13.57% in HbAA, and the difference is significant (χ2 = 4.61, P = 0.032). Multiplicity of infection was lower in HbAS gametocyte carriers (median = 2 genotypes/carrier in HbAS versus 3.5 genotypes/carrier in HbAA, Wilcoxon sum rank test = 188, P = 0.032). Gametocyte densities in the blood donor significantly influenced mosquito infection prevalence in both HbAS and HbAA individuals. The HbAS genotype had no significant effect on mosquito infection outcomes when using immune or naïve serum in feeding assays. In AB replacement feeding experiments, the odds ratio of mosquito infection for HbAA blood as compared to HbAS was 0.56 (95% CI 0.29–1.10), indicating a twice higher risk of infection in mosquitoes fed on gametocyte-containing blood of HbAS genotype. Conclusion Plasmodium transmission stages were more prevalent in SCT individuals. This may reflect the parasite’s enhanced investment in the sexual stage to increase their survival rate when asexual replication is impeded. The public health impact of our results points the need for intensive malaria control interventions in areas with high prevalence of HbAS. The similar infection parameters in feeding experiments where mosquitoes received the original serum from the blood donor indicated that immune responses to gametocyte surface proteins occur in both HbAS and HbAA individuals. The higher risk of infection in mosquitoes fed on HbAS blood depleted of immune factors suggests that changes in the membrane properties in HbAS erythrocytes may impact on the maturation process of gametocytes within circulating red blood cells. |
| first_indexed | 2024-04-09T12:51:49Z |
| format | Article |
| id | doaj.art-921c30f6ebb44504a7d7fa2af8cf1dce |
| institution | Directory Open Access Journal |
| issn | 1471-2334 |
| language | English |
| last_indexed | 2024-04-09T12:51:49Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Infectious Diseases |
| spelling | doaj.art-921c30f6ebb44504a7d7fa2af8cf1dce2023-05-14T11:09:56ZengBMCBMC Infectious Diseases1471-23342023-05-0123111110.1186/s12879-023-08134-xInfluence of the sickle cell trait on Plasmodium falciparum infectivity from naturally infected gametocyte carriersChristelle M. Ngou0Albert N. Bayibéki1Luc Abate2Olesula S. Makinde3Lionel B. Feufack-Donfack4Elangwe M. Sarah-Matio5Aline G. Bouopda-Tuedom6Paul Taconet7Nicolas Moiroux8Parfait H. Awono-Ambéné9Arthur Talman10Lawrence S. Ayong11Antoine Berry12Sandrine E. Nsango13Isabelle Morlais14Institut de Recherche pour le Développement, MIVEGEC, Univ. Montpellier, CNRS, IRDUniversité Catholique d’Afrique CentraleInstitut de Recherche pour le Développement, MIVEGEC, Univ. Montpellier, CNRS, IRDDepartment of Statistics, Federal University of TechnologyMalaria Research Unit, Centre Pasteur du CamerounInstitut de Recherche pour le Développement, MIVEGEC, Univ. Montpellier, CNRS, IRDMalaria Research Unit, Centre Pasteur du CamerounInstitut de Recherche pour le Développement, MIVEGEC, Univ. Montpellier, CNRS, IRDInstitut de Recherche pour le Développement, MIVEGEC, Univ. Montpellier, CNRS, IRDLaboratoire d’Entomologie Médicale, OCEACInstitut de Recherche pour le Développement, MIVEGEC, Univ. Montpellier, CNRS, IRDMalaria Research Unit, Centre Pasteur du CamerounInstitut Toulousain des Maladies Infectieuses et Inflammatoires (Infinity), Université Toulouse, CNRS UMR5051, INSERM UMR1291, UPSMalaria Research Unit, Centre Pasteur du CamerounInstitut de Recherche pour le Développement, MIVEGEC, Univ. Montpellier, CNRS, IRDAbstract Background Sickle cell trait (SCT) refers to the carriage of one abnormal copy of the β-globin gene, the HbS allele. SCT offers protection against malaria, controlling parasite density and preventing progression to symptomatic malaria. However, it remains unclear whether SCT also affects transmission stages and mosquito infection parameters. Deciphering the impact of the SCT on human to mosquito malaria transmission is key to understanding mechanisms that maintain the trait in malaria endemic areas. Methods The study was conducted from June to July 2017 among asymptomatic children living in the locality of Mfou, Cameroon. Blood samples were collected from asymptomatic children to perform malaria diagnosis by microscopy, Plasmodium species by PCR and hemoglobin typing by RFLP. Infectiousness of gametocytes to mosquitoes was assessed by membrane feeding assays using blood from gametocyte carriers of HbAA and HbAS genotypes. A zero-inflated model was fitted to predict distribution of oocysts in mosquitoes according to hemoglobin genotype of the gametocyte source. Results Among the 1557 children enrolled in the study, 314 (20.16%) were of the HbAS genotype. The prevalence of children with P. falciparum gametocytes was 18.47% in HbAS individuals and 13.57% in HbAA, and the difference is significant (χ2 = 4.61, P = 0.032). Multiplicity of infection was lower in HbAS gametocyte carriers (median = 2 genotypes/carrier in HbAS versus 3.5 genotypes/carrier in HbAA, Wilcoxon sum rank test = 188, P = 0.032). Gametocyte densities in the blood donor significantly influenced mosquito infection prevalence in both HbAS and HbAA individuals. The HbAS genotype had no significant effect on mosquito infection outcomes when using immune or naïve serum in feeding assays. In AB replacement feeding experiments, the odds ratio of mosquito infection for HbAA blood as compared to HbAS was 0.56 (95% CI 0.29–1.10), indicating a twice higher risk of infection in mosquitoes fed on gametocyte-containing blood of HbAS genotype. Conclusion Plasmodium transmission stages were more prevalent in SCT individuals. This may reflect the parasite’s enhanced investment in the sexual stage to increase their survival rate when asexual replication is impeded. The public health impact of our results points the need for intensive malaria control interventions in areas with high prevalence of HbAS. The similar infection parameters in feeding experiments where mosquitoes received the original serum from the blood donor indicated that immune responses to gametocyte surface proteins occur in both HbAS and HbAA individuals. The higher risk of infection in mosquitoes fed on HbAS blood depleted of immune factors suggests that changes in the membrane properties in HbAS erythrocytes may impact on the maturation process of gametocytes within circulating red blood cells.https://doi.org/10.1186/s12879-023-08134-xSickle cell traitAsymptomatic carriersMalaria transmissionMosquito infectivityGametocytes |
| spellingShingle | Christelle M. Ngou Albert N. Bayibéki Luc Abate Olesula S. Makinde Lionel B. Feufack-Donfack Elangwe M. Sarah-Matio Aline G. Bouopda-Tuedom Paul Taconet Nicolas Moiroux Parfait H. Awono-Ambéné Arthur Talman Lawrence S. Ayong Antoine Berry Sandrine E. Nsango Isabelle Morlais Influence of the sickle cell trait on Plasmodium falciparum infectivity from naturally infected gametocyte carriers BMC Infectious Diseases Sickle cell trait Asymptomatic carriers Malaria transmission Mosquito infectivity Gametocytes |
| title | Influence of the sickle cell trait on Plasmodium falciparum infectivity from naturally infected gametocyte carriers |
| title_full | Influence of the sickle cell trait on Plasmodium falciparum infectivity from naturally infected gametocyte carriers |
| title_fullStr | Influence of the sickle cell trait on Plasmodium falciparum infectivity from naturally infected gametocyte carriers |
| title_full_unstemmed | Influence of the sickle cell trait on Plasmodium falciparum infectivity from naturally infected gametocyte carriers |
| title_short | Influence of the sickle cell trait on Plasmodium falciparum infectivity from naturally infected gametocyte carriers |
| title_sort | influence of the sickle cell trait on plasmodium falciparum infectivity from naturally infected gametocyte carriers |
| topic | Sickle cell trait Asymptomatic carriers Malaria transmission Mosquito infectivity Gametocytes |
| url | https://doi.org/10.1186/s12879-023-08134-x |
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