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Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Malaria | Research

Diversity and immune responses against Plasmodium falciparum gametocytes in non-febrile school children living in Southern Ghana

Authors: Linda E. Amoah, Hamza B. Abagna, Ruth Ayanful-Torgby, Samuel O. Blankson, Nii A. Aryee

Published in: Malaria Journal | Issue 1/2019

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Abstract

Background

Natural exposure to gametocytes can result in the development of immunity against the gametocyte by the host as well as genetic diversity in the gametocyte. This study evaluated the quantity and quality of natural immune responses against a gametocyte antigen, Pfs230 as well as the prevalence and diversity of gametocytes circulating in children living in two communities in southern Ghana.

Methods

Whole blood (2.5 ml) was collected from 137 non-febrile school children aged between 6 and 12 years old quarterly for a 6-month period. A drop of blood was used to prepare thick and thin blood films for parasite prevalence and density estimation. Subsequently, stored plasma samples were used in ELISAs assays to measure antibody responses and avidity against Pfs230. RNA was extraction from Trizol preserved packed cells and subsequently converted to complementary DNA (cDNA) which was used for reverse transcriptase PCR (RT-PCR) to determine gametocytes prevalence and diversity.

Results

Gametocyte carriage in the peak season (July) determined by Pfg377 RT-PCR was 49.2% in Obom and 22.2% in Abura, and was higher than that determined by microscopy. Gametocyte diversity was low and predominated by the same allele at both sites. The relative avidity index for antibodies measured in Abura was higher than that recorded in Obom at all time points although Pfs230 IgG concentrations were significantly high (P < 0.0001) in Obom than in Abura at all time points. The IgG responses in Obom were significantly higher than that in Abura during the peak season.

Conclusion

Naturally induced antibody responses against Pfs230 in children living in both high perennial and low seasonal malaria transmission settings reduced significantly in moving from the peak to the off-peak season. The relative avidity of antibodies against Pfs230 in Abura was significantly higher than those measured in Obom, despite having lower IgG levels. Very limited diversity was identified in the gametocytes circulating in both Obom and Abura.
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Literature
1.
go back to reference NMCP. Annual Report. Ghana 2017. Ghana Health Services, Accra, 2018. NMCP. Annual Report. Ghana 2017. Ghana Health Services, Accra, 2018.
2.
go back to reference World Health Organization. World Malaria Report 2018. Geneva: World Health Organization; 2018.CrossRef World Health Organization. World Malaria Report 2018. Geneva: World Health Organization; 2018.CrossRef
3.
go back to reference Ayanful-Torgby R, Quashie NB, Boampong JN, Williamson KC, Amoah LE. Seasonal variations in Plasmodium falciparum parasite prevalence assessed by varying diagnostic tests in asymptomatic children in southern Ghana. PLoS ONE. 2018;13:e0199172.CrossRef Ayanful-Torgby R, Quashie NB, Boampong JN, Williamson KC, Amoah LE. Seasonal variations in Plasmodium falciparum parasite prevalence assessed by varying diagnostic tests in asymptomatic children in southern Ghana. PLoS ONE. 2018;13:e0199172.CrossRef
4.
go back to reference Abukari Z, Okonu R, Nyarko SB, Lo AC, Dieng CC, Salifu SP, et al. The diversity, multiplicity of infection and population structure of P. falciparum parasites circulating in asymptomatic carriers living in high and low malaria transmission settings of Ghana. Genes (Basel). 2019;10:E434.CrossRef Abukari Z, Okonu R, Nyarko SB, Lo AC, Dieng CC, Salifu SP, et al. The diversity, multiplicity of infection and population structure of P. falciparum parasites circulating in asymptomatic carriers living in high and low malaria transmission settings of Ghana. Genes (Basel). 2019;10:E434.CrossRef
5.
go back to reference Amoah LE, Acquah FK, Ayanful-Torgby R, Oppong A, Abankwa J, Obboh EK, et al. Dynamics of anti-MSP3 and Pfs230 antibody responses and multiplicity of infection in asymptomatic children from southern Ghana. Parasit Vectors. 2018;11:13.CrossRef Amoah LE, Acquah FK, Ayanful-Torgby R, Oppong A, Abankwa J, Obboh EK, et al. Dynamics of anti-MSP3 and Pfs230 antibody responses and multiplicity of infection in asymptomatic children from southern Ghana. Parasit Vectors. 2018;11:13.CrossRef
6.
go back to reference Acquah FK, Obboh EK, Asare K, Boampong JN, Nuvor SV, Singh SK, et al. Antibody responses to two new Lactococcus lactis-produced recombinant Pfs48/45 and Pfs230 proteins increase with age in malaria patients living in the Central Region of Ghana. Malar J. 2017;16:306.CrossRef Acquah FK, Obboh EK, Asare K, Boampong JN, Nuvor SV, Singh SK, et al. Antibody responses to two new Lactococcus lactis-produced recombinant Pfs48/45 and Pfs230 proteins increase with age in malaria patients living in the Central Region of Ghana. Malar J. 2017;16:306.CrossRef
7.
go back to reference Amoah LE, Nuvor SV, Obboh EK, Acquah FK, Asare K, Singh SK, et al. Natural antibody responses to Plasmodium falciparum MSP3 and GLURP(R0) antigens are associated with low parasite densities in malaria patients living in the Central Region of Ghana. Parasit Vectors. 2017;10:395.CrossRef Amoah LE, Nuvor SV, Obboh EK, Acquah FK, Asare K, Singh SK, et al. Natural antibody responses to Plasmodium falciparum MSP3 and GLURP(R0) antigens are associated with low parasite densities in malaria patients living in the Central Region of Ghana. Parasit Vectors. 2017;10:395.CrossRef
8.
go back to reference Menegon M, Severini C, Sannella A, Paglia MG, Sangare D, Abdel-Wahab A, et al. Genotyping of Plasmodium falciparum gametocytes by reverse transcriptase polymerase chain reaction. Mol Biochem Parasitol. 2000;111:153–61.CrossRef Menegon M, Severini C, Sannella A, Paglia MG, Sangare D, Abdel-Wahab A, et al. Genotyping of Plasmodium falciparum gametocytes by reverse transcriptase polymerase chain reaction. Mol Biochem Parasitol. 2000;111:153–61.CrossRef
9.
go back to reference Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006;22:424–30.CrossRef Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA. The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006;22:424–30.CrossRef
10.
go back to reference Barry AE, Arnott A. Strategies for designing and monitoring malaria vaccines targeting diverse antigens. Front Immunol. 2014;5:359.CrossRef Barry AE, Arnott A. Strategies for designing and monitoring malaria vaccines targeting diverse antigens. Front Immunol. 2014;5:359.CrossRef
11.
go back to reference Takala SL, Plowe CV. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming ‘vaccine resistant malaria’. Parasite Immunol. 2009;31:560–73.CrossRef Takala SL, Plowe CV. Genetic diversity and malaria vaccine design, testing and efficacy: preventing and overcoming ‘vaccine resistant malaria’. Parasite Immunol. 2009;31:560–73.CrossRef
12.
go back to reference Nakazawa S, Culleton R, Maeno Y. In vivo and in vitro gametocyte production of Plasmodium falciparum isolates from Northern Thailand. Int J Parasitol. 2011;41:317–23.CrossRef Nakazawa S, Culleton R, Maeno Y. In vivo and in vitro gametocyte production of Plasmodium falciparum isolates from Northern Thailand. Int J Parasitol. 2011;41:317–23.CrossRef
13.
go back to reference Acquah FK, Adjah J, Williamson KC, Amoah LE. Transmission-blocking vaccines: old friends and new prospects. Infect Immun. 2019;87:e00775–818.CrossRef Acquah FK, Adjah J, Williamson KC, Amoah LE. Transmission-blocking vaccines: old friends and new prospects. Infect Immun. 2019;87:e00775–818.CrossRef
14.
go back to reference Adjah J, Fiadzoe B, Ayanful-Torgby R, Amoah LE. Seasonal variations in Plasmodium falciparum genetic diversity and multiplicity of infection in asymptomatic children living in southern Ghana. BMC Infect Dis. 2018;18:432.CrossRef Adjah J, Fiadzoe B, Ayanful-Torgby R, Amoah LE. Seasonal variations in Plasmodium falciparum genetic diversity and multiplicity of infection in asymptomatic children living in southern Ghana. BMC Infect Dis. 2018;18:432.CrossRef
15.
go back to reference WHO. Giemsa staining of malaria blood films. Malaria microscopy standard operating procedure—MM-SOP-07A2016. Geneva: World Health Organization; 2016. WHO. Giemsa staining of malaria blood films. Malaria microscopy standard operating procedure—MM-SOP-07A2016. Geneva: World Health Organization; 2016.
16.
go back to reference WHO. Malaria parasite counting. Geneva: World Health Organization; 2016. WHO. Malaria parasite counting. Geneva: World Health Organization; 2016.
17.
go back to reference Ayanful-Torgby R, Oppong A, Abankwa J, Acquah F, Williamson KC, Amoah LE. Plasmodium falciparum genotype and gametocyte prevalence in children with uncomplicated malaria in coastal Ghana. Malar J. 2016;15:592.CrossRef Ayanful-Torgby R, Oppong A, Abankwa J, Acquah F, Williamson KC, Amoah LE. Plasmodium falciparum genotype and gametocyte prevalence in children with uncomplicated malaria in coastal Ghana. Malar J. 2016;15:592.CrossRef
18.
go back to reference Abagna HB, Acquah FK, Okonu R, Aryee NA, Theisen M, Amoah LE. Assessment of the quality and quantity of naturally induced antibody responses to EBA175RIII-V in Ghanaian children living in two communities with varying malaria transmission patterns. Malar J. 2018;17:14.CrossRef Abagna HB, Acquah FK, Okonu R, Aryee NA, Theisen M, Amoah LE. Assessment of the quality and quantity of naturally induced antibody responses to EBA175RIII-V in Ghanaian children living in two communities with varying malaria transmission patterns. Malar J. 2018;17:14.CrossRef
19.
go back to reference Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SL, Carneiro I, et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA. 2005;102:5108–13.CrossRef Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SL, Carneiro I, et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci USA. 2005;102:5108–13.CrossRef
20.
go back to reference Kusi KA, Bosomprah S, Dodoo D, Kyei-Baafour E, Dickson EK, Mensah D, et al. Anti-sporozoite antibodies as alternative markers for malaria transmission intensity estimation. Malar J. 2014;13:103.CrossRef Kusi KA, Bosomprah S, Dodoo D, Kyei-Baafour E, Dickson EK, Mensah D, et al. Anti-sporozoite antibodies as alternative markers for malaria transmission intensity estimation. Malar J. 2014;13:103.CrossRef
21.
go back to reference Parr JB, Belson C, Patel JC, Hoffman IF, Kamthunzi P, Martinson F, et al. Estimation of Plasmodium falciparum transmission intensity in Lilongwe, Malawi, by microscopy, rapid diagnostic testing, and nucleic acid detection. Am J Trop Med Hyg. 2016;95:373–7.CrossRef Parr JB, Belson C, Patel JC, Hoffman IF, Kamthunzi P, Martinson F, et al. Estimation of Plasmodium falciparum transmission intensity in Lilongwe, Malawi, by microscopy, rapid diagnostic testing, and nucleic acid detection. Am J Trop Med Hyg. 2016;95:373–7.CrossRef
22.
go back to reference Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151–208.CrossRef Tusting LS, Bousema T, Smith DL, Drakeley C. Measuring changes in Plasmodium falciparum transmission: precision, accuracy and costs of metrics. Adv Parasitol. 2014;84:151–208.CrossRef
23.
go back to reference Smith T, Felger I, Tanner M, Beck HP. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans R Soc Trop Med Hyg. 1999;93(Suppl 1):59–64.CrossRef Smith T, Felger I, Tanner M, Beck HP. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans R Soc Trop Med Hyg. 1999;93(Suppl 1):59–64.CrossRef
24.
go back to reference Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377–410.CrossRef Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377–410.CrossRef
25.
go back to reference Niederwieser I, Felger I, Beck HP. Limited polymorphism in Plasmodium falciparum sexual-stage antigens. Am J Trop Med Hyg. 2001;64:9–11.CrossRef Niederwieser I, Felger I, Beck HP. Limited polymorphism in Plasmodium falciparum sexual-stage antigens. Am J Trop Med Hyg. 2001;64:9–11.CrossRef
26.
go back to reference Bousema JT, Drakeley CJ, Sauerwein RW. Sexual-stage antibody responses to P. falciparum in endemic populations. Curr Mol Med. 2006;6:223–9.CrossRef Bousema JT, Drakeley CJ, Sauerwein RW. Sexual-stage antibody responses to P. falciparum in endemic populations. Curr Mol Med. 2006;6:223–9.CrossRef
27.
go back to reference Franks S, Baton L, Tetteh K, Tongren E, Dewin D, Akanmori BD, et al. Genetic diversity and antigenic polymorphism in Plasmodium falciparum: extensive serological cross-reactivity between allelic variants of merozoite surface protein 2. Infect Immun. 2003;71:3485–95.CrossRef Franks S, Baton L, Tetteh K, Tongren E, Dewin D, Akanmori BD, et al. Genetic diversity and antigenic polymorphism in Plasmodium falciparum: extensive serological cross-reactivity between allelic variants of merozoite surface protein 2. Infect Immun. 2003;71:3485–95.CrossRef
Metadata
Title
Diversity and immune responses against Plasmodium falciparum gametocytes in non-febrile school children living in Southern Ghana
Authors
Linda E. Amoah
Hamza B. Abagna
Ruth Ayanful-Torgby
Samuel O. Blankson
Nii A. Aryee
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2895-7

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