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Published in: BMC Infectious Diseases 1/2018

Open Access 01-12-2018 | Research article

Seasonal variations in Plasmodium falciparum genetic diversity and multiplicity of infection in asymptomatic children living in southern Ghana

Authors: Joshua Adjah, Bless Fiadzoe, Ruth Ayanful-Torgby, Linda E. Amoah

Published in: BMC Infectious Diseases | Issue 1/2018

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Abstract

Background

Genetic diversity in Plasmodium falciparum (P. falciparum) parasites is a major hurdle to the control of malaria. This study monitored changes in the genetic diversity and the multiplicity of P. falciparum parasite infection in asymptomatic children living in southern Ghana at 3 month intervals between April 2015 and January 2016.

Methods

Filter paper blood spots (DBS) were collected quarterly from children living in Obom, a community with perennial malaria transmission and Abura, a community with seasonal malaria transmission. Genomic DNA was extracted from the DBS and used in polymerase chain reaction (PCR)-based genotyping of the merozoite surface protein 1 (msp 1) and merozoite surface protein 2 (msp 2) genes.

Results

Out of a total of 787 samples that were collected from the two study sites, 59.2% (466/787) tested positive for P. falciparum. The msp 1 and msp 2 genes were successfully amplified from 73.8% (344/466) and 82.5% (385/466) of the P. falciparum positive samples respectively. The geometric mean MOI in Abura ranged between 1.17 (95% CI: 1.08–1.28) and 1.48 (95% CI: 1.36–1.60) and was significantly lower (p < 0.01, Dunn’s multiple comparison test) than that determined in Obom, where the geometric mean MOI ranged between 1.82 (95% CI: 1.58–2.08) and 2.50 (95% CI: 2.33–2.678) over the study period. Whilst the msp 1 R033:MAD20:KI allelic family ratio was dynamic, the msp 2 3D7:FC27 allelic family ratio remained relatively stable across the changing seasons in both sites.

Conclusions

This study shows that seasonal variations in parasite diversity in these communities can be better estimated by msp 1 rather than msp 2 due to the constantly changing relative intra allelic frequencies observed in msp 1 and the fact that the dominance of any msp 2 allele was dependent on the transmission setting but not on the season as opposed to the dominance of any msp 1 allele, which was dependent on both the season and the transmission setting.
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Literature
1.
2.
go back to reference Konaté L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, Spiegel A, Trape J-F, Mercereau-Puijalon O. 5. Variation of plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Trans R Soc Trop Med Hyg. 1999;93:21–8.CrossRefPubMed Konaté L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, Spiegel A, Trape J-F, Mercereau-Puijalon O. 5. Variation of plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Trans R Soc Trop Med Hyg. 1999;93:21–8.CrossRefPubMed
3.
go back to reference Smith T, Beck H-P, Kitua A, Mwankusye S, Felger I, Fraser-Hurt N, Irion A, Alonso P, Teuscher T, Tanner M. 4. Age dependence of the multiplicity of plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Trans R Soc Trop Med Hyg. 1999;93:15–20.CrossRefPubMed Smith T, Beck H-P, Kitua A, Mwankusye S, Felger I, Fraser-Hurt N, Irion A, Alonso P, Teuscher T, Tanner M. 4. Age dependence of the multiplicity of plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Trans R Soc Trop Med Hyg. 1999;93:15–20.CrossRefPubMed
4.
go back to reference Ntoumi F, Contamin H, Rogier C, Bonnefoy S, Trape J-F, Mercereau-Puijalon O. Age-dependent carriage of multiple plasmodium falciparum merozoite surface antigen-2 alleles in asymptomatic malaria infections. Am J Trop Med Hyg. 1995;52(1):81–8.CrossRefPubMed Ntoumi F, Contamin H, Rogier C, Bonnefoy S, Trape J-F, Mercereau-Puijalon O. Age-dependent carriage of multiple plasmodium falciparum merozoite surface antigen-2 alleles in asymptomatic malaria infections. Am J Trop Med Hyg. 1995;52(1):81–8.CrossRefPubMed
5.
go back to reference Karl S, White MT, Milne GJ, Gurarie D, Hay SI, Barry AE, Felger I, Mueller I. Spatial effects on the multiplicity of plasmodium falciparum infections. PLoS One. 2016;11(10):e0164054.CrossRefPubMedPubMedCentral Karl S, White MT, Milne GJ, Gurarie D, Hay SI, Barry AE, Felger I, Mueller I. Spatial effects on the multiplicity of plasmodium falciparum infections. PLoS One. 2016;11(10):e0164054.CrossRefPubMedPubMedCentral
6.
go back to reference Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, Magill AJ, X-z S. Genetic diversity and chloroquine selective sweeps in plasmodium falciparum. Nature. 2002;418(6895):320–3.CrossRefPubMed Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, Magill AJ, X-z S. Genetic diversity and chloroquine selective sweeps in plasmodium falciparum. Nature. 2002;418(6895):320–3.CrossRefPubMed
9.
go back to reference Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, Sitthi-amorn C, Renaud F, Harnyuttanakorn P. Genetic diversity and population structure of plasmodium falciparum in Thailand, a low transmission country. Malar J. 2009;8(1):155.CrossRefPubMedPubMedCentral Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, Sitthi-amorn C, Renaud F, Harnyuttanakorn P. Genetic diversity and population structure of plasmodium falciparum in Thailand, a low transmission country. Malar J. 2009;8(1):155.CrossRefPubMedPubMedCentral
10.
go back to reference Anderson TJ, Haubold B, Williams JT, Estrada-Franco § JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N. Microsatellite markers reveal a spectrum of population structures in the malaria parasite plasmodium falciparum. Mol Biol Evol. 2000;17(10):1467–82.CrossRefPubMed Anderson TJ, Haubold B, Williams JT, Estrada-Franco § JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N. Microsatellite markers reveal a spectrum of population structures in the malaria parasite plasmodium falciparum. Mol Biol Evol. 2000;17(10):1467–82.CrossRefPubMed
11.
go back to reference Machado RL, voa MMP, Calvosa VS, Ferreira MU, Rossit AR, EJd S, Conway DJ. Genetic structure of plasmodium falciparum populations in the Brazilian Amazon region. J Infect Dis. 2004;190(9):1547–55.CrossRefPubMed Machado RL, voa MMP, Calvosa VS, Ferreira MU, Rossit AR, EJd S, Conway DJ. Genetic structure of plasmodium falciparum populations in the Brazilian Amazon region. J Infect Dis. 2004;190(9):1547–55.CrossRefPubMed
12.
go back to reference Mita T, Jombart T. Patterns and dynamics of genetic diversity in plasmodium falciparum: what past human migrations tell us about malaria. Parasitol Int. 2015;64(3):238–43.CrossRefPubMed Mita T, Jombart T. Patterns and dynamics of genetic diversity in plasmodium falciparum: what past human migrations tell us about malaria. Parasitol Int. 2015;64(3):238–43.CrossRefPubMed
13.
go back to reference Arnott A, Barry AE, Reeder JC. Understanding the population genetics of plasmodium vivax is essential for malaria control and elimination. Malar J. 2012;11(1):14.CrossRefPubMedPubMedCentral Arnott A, Barry AE, Reeder JC. Understanding the population genetics of plasmodium vivax is essential for malaria control and elimination. Malar J. 2012;11(1):14.CrossRefPubMedPubMedCentral
14.
go back to reference Haddad D, Snounou G, Mattei D, Enamorado IG, Figueroa J, Ståhl S, Berzins K. Limited genetic diversity of plasmodium falciparum in field isolates from Honduras. Am J Trop Med Hyg. 1999;60(1):30–4.CrossRefPubMed Haddad D, Snounou G, Mattei D, Enamorado IG, Figueroa J, Ståhl S, Berzins K. Limited genetic diversity of plasmodium falciparum in field isolates from Honduras. Am J Trop Med Hyg. 1999;60(1):30–4.CrossRefPubMed
15.
go back to reference Babiker HA, Lines J, Hill WG, Walliker D. Population structure of plasmodium falciparum in villages with different malaria endemicity in East Africa. Am J Trop Med Hyg. 1997;56(2):141–7.CrossRefPubMed Babiker HA, Lines J, Hill WG, Walliker D. Population structure of plasmodium falciparum in villages with different malaria endemicity in East Africa. Am J Trop Med Hyg. 1997;56(2):141–7.CrossRefPubMed
16.
go back to reference Peyerl-Hoffmann G, Jelinek T, Kilian A, Kabagambe G, Metzger W, Von Sonnenburg F. Genetic diversity of plasmodium falciparum and its relationship to parasite density in an area with different malaria endemicities in West Uganda. Tropical Med Int Health. 2001;6(8):607–13.CrossRef Peyerl-Hoffmann G, Jelinek T, Kilian A, Kabagambe G, Metzger W, Von Sonnenburg F. Genetic diversity of plasmodium falciparum and its relationship to parasite density in an area with different malaria endemicities in West Uganda. Tropical Med Int Health. 2001;6(8):607–13.CrossRef
17.
go back to reference Babiker HA, Ranford-Cartwright LC, Walliker D. 3. Genetic structure and dynamics of plasmodium falciparum infections in the Kilombero region of Tanzania. Trans R Soc Trop Med Hyg. 1999;93:11–4.CrossRefPubMed Babiker HA, Ranford-Cartwright LC, Walliker D. 3. Genetic structure and dynamics of plasmodium falciparum infections in the Kilombero region of Tanzania. Trans R Soc Trop Med Hyg. 1999;93:11–4.CrossRefPubMed
18.
19.
go back to reference Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Path. 2012;8(4):e1002588.CrossRef Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Path. 2012;8(4):e1002588.CrossRef
20.
21.
go back to reference Srimath-Tirumula RCPK, Neelapu NRR, Sidagam N. Association of climatic variability, vector population and malarial disease in district of Visakhapatnam, India: a modeling and prediction analysis. PLoS One. 2015;10(6):e0128377.CrossRef Srimath-Tirumula RCPK, Neelapu NRR, Sidagam N. Association of climatic variability, vector population and malarial disease in district of Visakhapatnam, India: a modeling and prediction analysis. PLoS One. 2015;10(6):e0128377.CrossRef
22.
go back to reference Ntoumi F, Ngoundou-Landji J, Luty A, Dubreuil G, Millet P. Allelic polymorphism of plasmodium falciparum MSP-2 gene in blood samples from Gabonese children. Bull Soc Pathol Exot. 2001;94(2 Pt 2):183–7.PubMed Ntoumi F, Ngoundou-Landji J, Luty A, Dubreuil G, Millet P. Allelic polymorphism of plasmodium falciparum MSP-2 gene in blood samples from Gabonese children. Bull Soc Pathol Exot. 2001;94(2 Pt 2):183–7.PubMed
23.
go back to reference Krogstad DJ, Koita OA, Diallo M, Gerone JL, Poudiougou B, Diakité M, Touré YT. Molecular incidence and clearance of plasmodium falciparum infection. Malar J. 2015;14(1):415.CrossRefPubMedPubMedCentral Krogstad DJ, Koita OA, Diallo M, Gerone JL, Poudiougou B, Diakité M, Touré YT. Molecular incidence and clearance of plasmodium falciparum infection. Malar J. 2015;14(1):415.CrossRefPubMedPubMedCentral
24.
go back to reference Auburn S, Campino S, Miotto O, Djimde AA, Zongo I, Manske M, Maslen G, Mangano V, Alcock D, MacInnis B. Characterization of within-host plasmodium falciparum diversity using next-generation sequence data. PLoS One. 2012;7(2):e32891.CrossRefPubMedPubMedCentral Auburn S, Campino S, Miotto O, Djimde AA, Zongo I, Manske M, Maslen G, Mangano V, Alcock D, MacInnis B. Characterization of within-host plasmodium falciparum diversity using next-generation sequence data. PLoS One. 2012;7(2):e32891.CrossRefPubMedPubMedCentral
25.
go back to reference Viriyakosol S, Siripoon N, Petcharapirat C, Petcharapirat P, Jarra W, Thaithong S, Brown K, Snounou G. Genotyping of Plasmodium falciparum isolates by the polymerase chain reaction and potential uses in epidemiological studies. Bull World Health Organ. 1995;73(1):85.PubMedPubMedCentral Viriyakosol S, Siripoon N, Petcharapirat C, Petcharapirat P, Jarra W, Thaithong S, Brown K, Snounou G. Genotyping of Plasmodium falciparum isolates by the polymerase chain reaction and potential uses in epidemiological studies. Bull World Health Organ. 1995;73(1):85.PubMedPubMedCentral
26.
go back to reference Dobaño C, Rogerson SJ, Taylor TE, McBride JS, Molyneux ME. Expression of merozoite surface protein markers by plasmodium falciparum-infected erythrocytes in peripheral blood and tissues of children with fatal malaria. Infect Immun. 2007;75(2):643–52.CrossRefPubMed Dobaño C, Rogerson SJ, Taylor TE, McBride JS, Molyneux ME. Expression of merozoite surface protein markers by plasmodium falciparum-infected erythrocytes in peripheral blood and tissues of children with fatal malaria. Infect Immun. 2007;75(2):643–52.CrossRefPubMed
27.
go back to reference Organization WH. Methods and techniques for clinical trials on antimalarial drug efficacy: genotyping to identify parasite populations: informal consultation organized by the Medicines for Malaria Venture and cosponsored by the World Health Organization, 29-31 May 2007, Amsterdam, The Netherlands. 2008. Organization WH. Methods and techniques for clinical trials on antimalarial drug efficacy: genotyping to identify parasite populations: informal consultation organized by the Medicines for Malaria Venture and cosponsored by the World Health Organization, 29-31 May 2007, Amsterdam, The Netherlands. 2008.
28.
go back to reference Botwe AK, Asante KP, Adjei G, Assafuah S, Dosoo D, Owusu-Agyei S. Dynamics in multiplicity of plasmodium falciparum infection among children with asymptomatic malaria in Central Ghana. BMC Genet. 2017;18(1):67.CrossRefPubMedPubMedCentral Botwe AK, Asante KP, Adjei G, Assafuah S, Dosoo D, Owusu-Agyei S. Dynamics in multiplicity of plasmodium falciparum infection among children with asymptomatic malaria in Central Ghana. BMC Genet. 2017;18(1):67.CrossRefPubMedPubMedCentral
29.
go back to reference Saha P, Ganguly S, Maji AK. Genetic diversity and multiplicity of infection of plasmodium falciparum isolates from Kolkata, West Bengal, India. Infect Genet Evol. 2016;43:239–44.CrossRefPubMed Saha P, Ganguly S, Maji AK. Genetic diversity and multiplicity of infection of plasmodium falciparum isolates from Kolkata, West Bengal, India. Infect Genet Evol. 2016;43:239–44.CrossRefPubMed
30.
go back to reference Soe TN, Wu Y, Tun MW, Xu X, Hu Y, Ruan Y, Win AYN, Nyunt MH, Mon NCN, Han KT. Genetic diversity of plasmodium falciparum populations in southeast and western Myanmar. Parasit Vectors. 2017;10(1):322.CrossRefPubMedPubMedCentral Soe TN, Wu Y, Tun MW, Xu X, Hu Y, Ruan Y, Win AYN, Nyunt MH, Mon NCN, Han KT. Genetic diversity of plasmodium falciparum populations in southeast and western Myanmar. Parasit Vectors. 2017;10(1):322.CrossRefPubMedPubMedCentral
32.
go back to reference Stoler J, Delimini RK, Bonney JK, Oduro AR, Owusu-Agyei S, Fobil JN, Awandare GA. Evidence of recent dengue exposure among malaria parasite-positive children in three urban centers in Ghana. Am J Trop Med Hyg. 2015;92(3):497–500.CrossRefPubMedPubMedCentral Stoler J, Delimini RK, Bonney JK, Oduro AR, Owusu-Agyei S, Fobil JN, Awandare GA. Evidence of recent dengue exposure among malaria parasite-positive children in three urban centers in Ghana. Am J Trop Med Hyg. 2015;92(3):497–500.CrossRefPubMedPubMedCentral
34.
go back to reference Duah NO, Matrevi SA, Quashie NB, Abuaku B, Koram KA. Genetic diversity of plasmodium falciparum isolates from uncomplicated malaria cases in Ghana over a decade. Parasit Vectors. 2016;9(1):416.CrossRefPubMedPubMedCentral Duah NO, Matrevi SA, Quashie NB, Abuaku B, Koram KA. Genetic diversity of plasmodium falciparum isolates from uncomplicated malaria cases in Ghana over a decade. Parasit Vectors. 2016;9(1):416.CrossRefPubMedPubMedCentral
35.
go back to reference Kateera F, Nsobya SL, Tukwasibwe S, Mens PF, Hakizimana E, Grobusch MP, Mutesa L, Kumar N, Vugt M. Malaria case clinical profiles and plasmodium falciparum parasite genetic diversity: a cross sectional survey at two sites of different malaria transmission intensities in Rwanda. Malar J. 2016;15(1):237.CrossRefPubMedPubMedCentral Kateera F, Nsobya SL, Tukwasibwe S, Mens PF, Hakizimana E, Grobusch MP, Mutesa L, Kumar N, Vugt M. Malaria case clinical profiles and plasmodium falciparum parasite genetic diversity: a cross sectional survey at two sites of different malaria transmission intensities in Rwanda. Malar J. 2016;15(1):237.CrossRefPubMedPubMedCentral
36.
go back to reference Amoah LE, Acquah FK, Ayanful-Torgby R, Oppong A, Abankwa J, Obboh EK, Singh SK, Theisen M. Dynamics of anti-MSP3 and Pfs230 antibody responses and multiplicity of infection in asymptomatic children from southern Ghana. Parasit Vectors. 2018;11(1):13.CrossRefPubMedPubMedCentral Amoah LE, Acquah FK, Ayanful-Torgby R, Oppong A, Abankwa J, Obboh EK, Singh SK, Theisen M. Dynamics of anti-MSP3 and Pfs230 antibody responses and multiplicity of infection in asymptomatic children from southern Ghana. Parasit Vectors. 2018;11(1):13.CrossRefPubMedPubMedCentral
37.
go back to reference Service GS. Cape Coast Municipality. In: 2010 Population & Housing Consensus: District Analytical Report. Ghana; 2014. Service GS. Cape Coast Municipality. In: 2010 Population & Housing Consensus: District Analytical Report. Ghana; 2014.
38.
go back to reference Service GS. Ga South Municipality. In: 2010 Population & Housing Consensus: District Analytical Report. Ghana; 2014. Service GS. Ga South Municipality. In: 2010 Population & Housing Consensus: District Analytical Report. Ghana; 2014.
39.
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(1):592.CrossRefPubMedPubMedCentral 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(1):592.CrossRefPubMedPubMedCentral
40.
go back to reference Musapa M, Kumwenda T, Mkulama M, Chishimba S, Norris DE, Thuma PE, Mharakurwa S. A simple Chelex protocol for DNA extraction from Anopheles spp. J Vis Exp. 2013;71:e3281. Musapa M, Kumwenda T, Mkulama M, Chishimba S, Norris DE, Thuma PE, Mharakurwa S. A simple Chelex protocol for DNA extraction from Anopheles spp. J Vis Exp. 2013;71:e3281.
41.
go back to reference Amoah LE, Nuvor SV, Obboh EK, Acquah FK, Asare K, Singh SK, Boampong JN, Theisen M, Williamson KC. 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(1):395.CrossRefPubMedPubMedCentral Amoah LE, Nuvor SV, Obboh EK, Acquah FK, Asare K, Singh SK, Boampong JN, Theisen M, Williamson KC. 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(1):395.CrossRefPubMedPubMedCentral
42.
go back to reference Boonma P, Christensen PR, Suwanarusk R, Price RN, Russell B. Comparison of three molecular methods for the detection and speciation of plasmodium vivax and plasmodium falciparum. Malar J. 2007;6(1):124.CrossRefPubMedPubMedCentral Boonma P, Christensen PR, Suwanarusk R, Price RN, Russell B. Comparison of three molecular methods for the detection and speciation of plasmodium vivax and plasmodium falciparum. Malar J. 2007;6(1):124.CrossRefPubMedPubMedCentral
43.
go back to reference Organization WH. Recommended genotyping procedures (RGPs) to identify parasite populations. In: Developed after an informal consultation organized by the Medicines for Malaria Venture and cosponsored by the World Health Organization; 2007. Organization WH. Recommended genotyping procedures (RGPs) to identify parasite populations. In: Developed after an informal consultation organized by the Medicines for Malaria Venture and cosponsored by the World Health Organization; 2007.
44.
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(1):14. https://doi.org/10.1186/s12936-017-2167-3. 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(1):14. https://​doi.​org/​10.​1186/​s12936-017-2167-3.
45.
go back to reference Kobbe R, Neuhoff R, Marks F, Adjei S, Langefeld I, Von Reden C, Adjei O, Meyer CG, May J. Seasonal variation and high multiplicity of first plasmodium falciparum infections in children from a holoendemic area in Ghana, West Africa. Tropical Med Int Health. 2006;11(5):613–9.CrossRef Kobbe R, Neuhoff R, Marks F, Adjei S, Langefeld I, Von Reden C, Adjei O, Meyer CG, May J. Seasonal variation and high multiplicity of first plasmodium falciparum infections in children from a holoendemic area in Ghana, West Africa. Tropical Med Int Health. 2006;11(5):613–9.CrossRef
46.
go back to reference Elissa N, Migot-Nabias F, Luty A, Renaut A, Toure F, Vaillant M, Lawoko M, Yangari P, Mayombo J, Lekoulou F, et al. Relationship between entomological inoculation rate, plasmodium falciparum prevalence rate, and incidence of malaria attack in rural Gabon. Acta Trop. 2003;85(3):355–61.CrossRefPubMed Elissa N, Migot-Nabias F, Luty A, Renaut A, Toure F, Vaillant M, Lawoko M, Yangari P, Mayombo J, Lekoulou F, et al. Relationship between entomological inoculation rate, plasmodium falciparum prevalence rate, and incidence of malaria attack in rural Gabon. Acta Trop. 2003;85(3):355–61.CrossRefPubMed
47.
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(6):e0199172.CrossRefPubMedPubMedCentral 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(6):e0199172.CrossRefPubMedPubMedCentral
48.
go back to reference Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I. Ultra-sensitive detection of plasmodium falciparum by amplification of multi-copy subtelomeric targets. PLoS Med. 2015;12(3):e1001788.CrossRefPubMedPubMedCentral Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I. Ultra-sensitive detection of plasmodium falciparum by amplification of multi-copy subtelomeric targets. PLoS Med. 2015;12(3):e1001788.CrossRefPubMedPubMedCentral
49.
go back to reference Das S, Muleba M, Stevenson JC, Pringle JC, Norris DE. Beyond the entomological inoculation rate: characterizing multiple blood feeding behavior and plasmodium falciparum multiplicity of infection in Anopheles mosquitoes in northern Zambia. Parasit Vectors. 2017;10(1):45.CrossRefPubMedPubMedCentral Das S, Muleba M, Stevenson JC, Pringle JC, Norris DE. Beyond the entomological inoculation rate: characterizing multiple blood feeding behavior and plasmodium falciparum multiplicity of infection in Anopheles mosquitoes in northern Zambia. Parasit Vectors. 2017;10(1):45.CrossRefPubMedPubMedCentral
50.
go back to reference Atroosh WM, Al-Mekhlafi HM, Mahdy MA, Saif-Ali R, Al-Mekhlafi AM, Surin J. Genetic diversity of plasmodium falciparum isolates from Pahang, Malaysia based on MSP-1 and MSP-2 genes. Parasit Vectors. 2011;4(1):233.CrossRefPubMedPubMedCentral Atroosh WM, Al-Mekhlafi HM, Mahdy MA, Saif-Ali R, Al-Mekhlafi AM, Surin J. Genetic diversity of plasmodium falciparum isolates from Pahang, Malaysia based on MSP-1 and MSP-2 genes. Parasit Vectors. 2011;4(1):233.CrossRefPubMedPubMedCentral
51.
go back to reference Mohammed H, Kassa M, Assefa A, Tadesse M, Kebede A. Genetic polymorphism of Merozoite surface Protein-2 (MSP-2) in plasmodium falciparum isolates from Pawe District, north West Ethiopia. PLoS One. 2017;12(5):e0177559.CrossRefPubMedPubMedCentral Mohammed H, Kassa M, Assefa A, Tadesse M, Kebede A. Genetic polymorphism of Merozoite surface Protein-2 (MSP-2) in plasmodium falciparum isolates from Pawe District, north West Ethiopia. PLoS One. 2017;12(5):e0177559.CrossRefPubMedPubMedCentral
52.
go back to reference Amoah LE, Opong A, Ayanful-Torgby R, Abankwa J, Acquah FK. Prevalence of G6PD deficiency and plasmodium falciparum parasites in asymptomatic school children living in southern Ghana. Malar J. 2016;15(1):388.CrossRefPubMedPubMedCentral Amoah LE, Opong A, Ayanful-Torgby R, Abankwa J, Acquah FK. Prevalence of G6PD deficiency and plasmodium falciparum parasites in asymptomatic school children living in southern Ghana. Malar J. 2016;15(1):388.CrossRefPubMedPubMedCentral
53.
go back to reference Agyeman-Budu A, Brown C, Adjei G, Adams M, Dosoo D, Dery D, Wilson M, Asante KP, Greenwood B, Owusu-Agyei S. Trends in multiplicity of plasmodium falciparum infections among asymptomatic residents in the middle belt of Ghana. Malar J. 2013;12(1):22.CrossRefPubMedPubMedCentral Agyeman-Budu A, Brown C, Adjei G, Adams M, Dosoo D, Dery D, Wilson M, Asante KP, Greenwood B, Owusu-Agyei S. Trends in multiplicity of plasmodium falciparum infections among asymptomatic residents in the middle belt of Ghana. Malar J. 2013;12(1):22.CrossRefPubMedPubMedCentral
54.
go back to reference Contamin H, Fandeur T, Bonnefoy S, Skouri F, Ntoumi F, Mercereau-Puijalon O. PCR typing of field isolates of plasmodium falciparum. J Clin Microbiol. 1995;33(4):944–51.PubMedPubMedCentral Contamin H, Fandeur T, Bonnefoy S, Skouri F, Ntoumi F, Mercereau-Puijalon O. PCR typing of field isolates of plasmodium falciparum. J Clin Microbiol. 1995;33(4):944–51.PubMedPubMedCentral
55.
go back to reference Magesa SM. Malaria Parasite Dynamics: Epidemiology, Allelic Diversity and Turnover Rates of Plasmodium falciparum Infections in Tanzanian Children: Ph. D. Thesis. Denmark: Department of Population Biology, Zoological Institute, University of Copenhagen; 1999. Magesa SM. Malaria Parasite Dynamics: Epidemiology, Allelic Diversity and Turnover Rates of Plasmodium falciparum Infections in Tanzanian Children: Ph. D. Thesis. Denmark: Department of Population Biology, Zoological Institute, University of Copenhagen; 1999.
56.
go back to reference Hamid MMA, Elamin AF, Albsheer MMA, Abdalla AA, Mahgoub NS, Mustafa SO, Muneer MS, Amin M. Multiplicity of infection and genetic diversity of plasmodium falciparum isolates from patients with uncomplicated and severe malaria in Gezira State, Sudan. Parasit Vectors. 2016;9(1):362.CrossRef Hamid MMA, Elamin AF, Albsheer MMA, Abdalla AA, Mahgoub NS, Mustafa SO, Muneer MS, Amin M. Multiplicity of infection and genetic diversity of plasmodium falciparum isolates from patients with uncomplicated and severe malaria in Gezira State, Sudan. Parasit Vectors. 2016;9(1):362.CrossRef
57.
go back to reference Hamid MMA, Mohammed SB, El Hassan IM. Genetic diversity of plasmodium falciparum field isolates in Central Sudan inferred by PCR genotyping of merozoite surface protein 1 and 2. N Am J Med Sci. 2013;5(2):95.CrossRefPubMedPubMedCentral Hamid MMA, Mohammed SB, El Hassan IM. Genetic diversity of plasmodium falciparum field isolates in Central Sudan inferred by PCR genotyping of merozoite surface protein 1 and 2. N Am J Med Sci. 2013;5(2):95.CrossRefPubMedPubMedCentral
58.
go back to reference Mohammed H, Mindaye T, Belayneh M, Kassa M, Assefa A, Tadesse M, Woyessa A, Mengesha T, Kebede A. Genetic diversity of plasmodium falciparum isolates based on MSP-1 and MSP-2 genes from Kolla-Shele area, Arbaminch Zuria District, Southwest Ethiopia. Malar J. 2015;14(1):73.CrossRefPubMedPubMedCentral Mohammed H, Mindaye T, Belayneh M, Kassa M, Assefa A, Tadesse M, Woyessa A, Mengesha T, Kebede A. Genetic diversity of plasmodium falciparum isolates based on MSP-1 and MSP-2 genes from Kolla-Shele area, Arbaminch Zuria District, Southwest Ethiopia. Malar J. 2015;14(1):73.CrossRefPubMedPubMedCentral
59.
go back to reference Hay SI, Sinka ME, Okara RM, Kabaria CW, Mbithi PM, Tago CC, Benz D, Gething PW, Howes RE, Patil AP. Developing global maps of the dominant Anopheles vectors of human malaria. PLoS Med. 2010;7(2):e1000209.CrossRefPubMedPubMedCentral Hay SI, Sinka ME, Okara RM, Kabaria CW, Mbithi PM, Tago CC, Benz D, Gething PW, Howes RE, Patil AP. Developing global maps of the dominant Anopheles vectors of human malaria. PLoS Med. 2010;7(2):e1000209.CrossRefPubMedPubMedCentral
Metadata
Title
Seasonal variations in Plasmodium falciparum genetic diversity and multiplicity of infection in asymptomatic children living in southern Ghana
Authors
Joshua Adjah
Bless Fiadzoe
Ruth Ayanful-Torgby
Linda E. Amoah
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-018-3350-z

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