Comparative analysis of asexual and sexual stage Plasmodium falciparum development in different red blood cell types

Abstract Background Red blood cell (RBC) polymorphisms are suggested to influence the course of Plasmodium falciparum malaria. Whereas some variants have been found to be protective, others have been found to enhance parasite development. This study evaluated the effect of variant haemoglobin (Hb) a...

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Main Authors: Linda E. Amoah, Festus K. Acquah, Prince B. Nyarko, Elizabeth Cudjoe, Dickson Donu, Ruth Ayanful-Torgby, Fredericka Sey, Kim C. Williamson, Gordon A. Awandare
Format: Article
Language:English
Published: BMC 2020-06-01
Series:Malaria Journal
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12936-020-03275-9
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spelling doaj-ad931e64cadd40da9832f8ae1858d40b2020-11-25T04:02:11ZengBMCMalaria Journal1475-28752020-06-0119111010.1186/s12936-020-03275-9Comparative analysis of asexual and sexual stage Plasmodium falciparum development in different red blood cell typesLinda E. Amoah0Festus K. Acquah1Prince B. Nyarko2Elizabeth Cudjoe3Dickson Donu4Ruth Ayanful-Torgby5Fredericka Sey6Kim C. Williamson7Gordon A. Awandare8Department of Immunology, Noguchi Memorial Institute for Medical Research, University of GhanaDepartment of Immunology, Noguchi Memorial Institute for Medical Research, University of GhanaWest African Centre for Cell Biology of Infectious Pathogens, University of GhanaDepartment of Immunology, Noguchi Memorial Institute for Medical Research, University of GhanaDepartment of Immunology, Noguchi Memorial Institute for Medical Research, University of GhanaDepartment of Immunology, Noguchi Memorial Institute for Medical Research, University of GhanaGhana Institute of Clinical GeneticsMicrobiology and Immunology Department, Uniformed Services University of the Health SciencesWest African Centre for Cell Biology of Infectious Pathogens, University of GhanaAbstract Background Red blood cell (RBC) polymorphisms are suggested to influence the course of Plasmodium falciparum malaria. Whereas some variants have been found to be protective, others have been found to enhance parasite development. This study evaluated the effect of variant haemoglobin (Hb) and ABO blood groups on P. falciparum merozoite invasion, multiplication rates as well as gametocyte development. Methods Approximately 2.5 mL of venous blood was collected from each participant. Flow cytometry was used to determine the in vitro merozoite invasion rates of NF54 parasites into the blood of 66 non-parasitaemic individuals with variant Hb genotypes (HbSS, HbSC) and blood groups (A, B, O), which were then compared with invasion into HbAA blood. The ex vivo asexual parasite multiplication and gametocyte production rates of parasites from 79 uncomplicated malaria patients with varying Hb genotypes (HbAS, HbAC and HbAA) were also estimated using microscopy. Results Merozoite invasion rates were significantly reduced by about 50% in RBCs containing HbSS and HbSC relative to HbAA cells. The presence of blood group O and B reduced the invasion rates of HbSS by about 50% and 60%, respectively, relative to HbSC but the presence of blood group A removed the inhibitory effect of HbSS. The initial parasite densities in uncomplicated malaria patients with Hb genotypes HbAS and HbAC cells were similar but significantly lower than those with genotype HbAA. The ex vivo parasite multiplication rate, gametocytaemia and gametocyte conversion rates followed a similar trend but did not reach statistical significance (p > 0.05). Conclusions Parasite invasion rate into erythrocytes is dependent on both erythrocyte blood group antigen and haemoglobin genotype as blood group O and B provided protection via reduced merozoite invasion in RBCs containing HbSS relative to HbSC. Regardless of haemoglobin type, greater than 70% malaria patients had circulating ring stage parasites that differentiated into stage II gametocytes in 4 days.http://link.springer.com/article/10.1186/s12936-020-03275-9HaemoglobinopathiesMalariaGametocyteMerozoite
collection DOAJ
language English
format Article
sources DOAJ
author Linda E. Amoah
Festus K. Acquah
Prince B. Nyarko
Elizabeth Cudjoe
Dickson Donu
Ruth Ayanful-Torgby
Fredericka Sey
Kim C. Williamson
Gordon A. Awandare
spellingShingle Linda E. Amoah
Festus K. Acquah
Prince B. Nyarko
Elizabeth Cudjoe
Dickson Donu
Ruth Ayanful-Torgby
Fredericka Sey
Kim C. Williamson
Gordon A. Awandare
Comparative analysis of asexual and sexual stage Plasmodium falciparum development in different red blood cell types
Malaria Journal
Haemoglobinopathies
Malaria
Gametocyte
Merozoite
author_facet Linda E. Amoah
Festus K. Acquah
Prince B. Nyarko
Elizabeth Cudjoe
Dickson Donu
Ruth Ayanful-Torgby
Fredericka Sey
Kim C. Williamson
Gordon A. Awandare
author_sort Linda E. Amoah
title Comparative analysis of asexual and sexual stage Plasmodium falciparum development in different red blood cell types
title_short Comparative analysis of asexual and sexual stage Plasmodium falciparum development in different red blood cell types
title_full Comparative analysis of asexual and sexual stage Plasmodium falciparum development in different red blood cell types
title_fullStr Comparative analysis of asexual and sexual stage Plasmodium falciparum development in different red blood cell types
title_full_unstemmed Comparative analysis of asexual and sexual stage Plasmodium falciparum development in different red blood cell types
title_sort comparative analysis of asexual and sexual stage plasmodium falciparum development in different red blood cell types
publisher BMC
series Malaria Journal
issn 1475-2875
publishDate 2020-06-01
description Abstract Background Red blood cell (RBC) polymorphisms are suggested to influence the course of Plasmodium falciparum malaria. Whereas some variants have been found to be protective, others have been found to enhance parasite development. This study evaluated the effect of variant haemoglobin (Hb) and ABO blood groups on P. falciparum merozoite invasion, multiplication rates as well as gametocyte development. Methods Approximately 2.5 mL of venous blood was collected from each participant. Flow cytometry was used to determine the in vitro merozoite invasion rates of NF54 parasites into the blood of 66 non-parasitaemic individuals with variant Hb genotypes (HbSS, HbSC) and blood groups (A, B, O), which were then compared with invasion into HbAA blood. The ex vivo asexual parasite multiplication and gametocyte production rates of parasites from 79 uncomplicated malaria patients with varying Hb genotypes (HbAS, HbAC and HbAA) were also estimated using microscopy. Results Merozoite invasion rates were significantly reduced by about 50% in RBCs containing HbSS and HbSC relative to HbAA cells. The presence of blood group O and B reduced the invasion rates of HbSS by about 50% and 60%, respectively, relative to HbSC but the presence of blood group A removed the inhibitory effect of HbSS. The initial parasite densities in uncomplicated malaria patients with Hb genotypes HbAS and HbAC cells were similar but significantly lower than those with genotype HbAA. The ex vivo parasite multiplication rate, gametocytaemia and gametocyte conversion rates followed a similar trend but did not reach statistical significance (p > 0.05). Conclusions Parasite invasion rate into erythrocytes is dependent on both erythrocyte blood group antigen and haemoglobin genotype as blood group O and B provided protection via reduced merozoite invasion in RBCs containing HbSS relative to HbSC. Regardless of haemoglobin type, greater than 70% malaria patients had circulating ring stage parasites that differentiated into stage II gametocytes in 4 days.
topic Haemoglobinopathies
Malaria
Gametocyte
Merozoite
url http://link.springer.com/article/10.1186/s12936-020-03275-9
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