Skip to main content
Top
Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Plasmodium Falciparum | Research

Genetic diversity of Plasmodium falciparum isolates from patients with uncomplicated and severe malaria based on msp-1 and msp-2 genes in Gublak, North West Ethiopia

Authors: Hussein Mohammed, Kedir Hassen, Ashenafi Assefa, Kalkidan Mekete, Gemechu Tadesse, Girum Taye, Robert J. Commons

Published in: Malaria Journal | Issue 1/2019

Login to get access

Abstract

Background

Malaria infection can present with a wide variety of symptoms, ranging from mild to severe. Plasmodium falciparum isolates in uncomplicated and severe malaria infections may have different parasite genetic profiles. This study was conducted to assess differences in genetic diversity and allelic frequencies in P. falciparum isolates according to malaria severity and age of patients in the Gublack area, northwest Ethiopia.

Methods

Cross-sectional health facility-based study conducted in Gublak, Ethiopia between July, 2017 and October, 2017. Symptomatic P. falciparum malaria patients with microscopically-confirmed infection were enrolled. Parasite DNA was extracted from filter paper blood spots and the polymorphic regions of the msp-1 and msp-2 genes were genotyped using allele-specific nested-PCR with fragment analysis by gel electrophoresis.

Results

A total of 118 patients were enrolled including 95 (80.5%) with uncomplicated infection and 23 (19.5%) with severe disease. In msp-1, the K1 allelic family was similarly prevalent in uncomplicated 42 (44.2%) and severe disease 12 (52.2%). In msp-2, FC27 was detected in 55 (57.9%) of uncomplicated infections and IC/3D7 in 14 (60.9%) of severe infections. 76 (64.4%) of the 118 isolates contained multiple genotypes; 56 (58.9%) in uncomplicated infections and 19 (82.6%) in severe infections. The overall of multiplicity of infection was 2.2 (95% CI 1.98–2.42) with 1.4 (95% CI 1.23–1.55) and 1.7 (95% CI 1.49–1.86) for msp-1 and msp-2, respectively. Multiplicity of infection was significantly higher in severe than uncomplicated infections (3.0 (95% CI 2.61–3.47) versus 2.0 (95% CI 1.83–2.23), respectively, p = 0.001). There was no difference in multiplicity of infection across age groups (p = 0.104).

Conclusion

Patients with severe malaria were more likely to have multiclonal infections. Further studies are needed to describe the association between P. falciparum genotypes and malaria severity in different malaria transmission areas.
Appendix
Available only for authorised users
Literature
2.
go back to reference Ayalew S, Mamo H, Animut A, Erko B. Assessment of current malaria status in light of the ongoing control interventions, socio-demographic and environmental variables in Jiga area, northwest Ethiopia. PLoS ONE. 2016;11:e0146214.PubMedPubMedCentralCrossRef Ayalew S, Mamo H, Animut A, Erko B. Assessment of current malaria status in light of the ongoing control interventions, socio-demographic and environmental variables in Jiga area, northwest Ethiopia. PLoS ONE. 2016;11:e0146214.PubMedPubMedCentralCrossRef
3.
go back to reference Federal Democratic Republic of Ethiopia Ministry of Health. National strategic plan for malaria prevention, control and elimination in Ethiopia, 2011–2015. Addis Ababa, Ethiopia; 2015. Federal Democratic Republic of Ethiopia Ministry of Health. National strategic plan for malaria prevention, control and elimination in Ethiopia, 2011–2015. Addis Ababa, Ethiopia; 2015.
5.
go back to reference WHO. Severe malaria. Trop Med Int Health. 2014;19(suppl 1):7–131. WHO. Severe malaria. Trop Med Int Health. 2014;19(suppl 1):7–131.
6.
go back to reference Reyburn H, Mbatia R, Drakeley C, Bruce J, Carneiro I, Olomi R, Cox J, et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA. 2005;293:1461–70.PubMedCrossRef Reyburn H, Mbatia R, Drakeley C, Bruce J, Carneiro I, Olomi R, Cox J, et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA. 2005;293:1461–70.PubMedCrossRef
7.
go back to reference Pasvol G. Cell-cell interaction in the pathogenesis of severe falciparum malaria. Clin Med J. 2001;1:495–500.CrossRef Pasvol G. Cell-cell interaction in the pathogenesis of severe falciparum malaria. Clin Med J. 2001;1:495–500.CrossRef
8.
go back to reference Kiwuwa MS, Ribacke U, Moll K, Byarugaba J, Lundblom K, Färnert A, et al. Genetic diversity of Plasmodium falciparum infections in mild and severe malaria of children from Kampala, Uganda. Parasitol Res. 2013;112:1691–700.PubMedPubMedCentralCrossRef Kiwuwa MS, Ribacke U, Moll K, Byarugaba J, Lundblom K, Färnert A, et al. Genetic diversity of Plasmodium falciparum infections in mild and severe malaria of children from Kampala, Uganda. Parasitol Res. 2013;112:1691–700.PubMedPubMedCentralCrossRef
9.
go back to reference A-Elbasit IE, ElGhazali G, A-Elgadir TM, Hamad AA, Babiker HA, Elbashir MI, et al. Allelic polymorphism of MSP2 gene in severe P. falciparum malaria in an area of low and seasonal transmission. Parasitol Res. 2007;102:29–34.PubMedCrossRef A-Elbasit IE, ElGhazali G, A-Elgadir TM, Hamad AA, Babiker HA, Elbashir MI, et al. Allelic polymorphism of MSP2 gene in severe P. falciparum malaria in an area of low and seasonal transmission. Parasitol Res. 2007;102:29–34.PubMedCrossRef
10.
go back to reference Bob NS, Diop BM, Renaud F, Marrama L, Durand P, Tall A, et al. Parasite polymorphism and severe malaria in Dakar (Senegal): a West African urban area. PLoS ONE. 2010;5(9817):e9817.PubMedPubMedCentralCrossRef Bob NS, Diop BM, Renaud F, Marrama L, Durand P, Tall A, et al. Parasite polymorphism and severe malaria in Dakar (Senegal): a West African urban area. PLoS ONE. 2010;5(9817):e9817.PubMedPubMedCentralCrossRef
11.
go back to reference Rout R, Mohapatra BN, Kar SK, Ranjit M. Genetic complexity and transmissibility of Plasmodium falciparum parasites causing severe malaria in central-east coast India. Trop Biomed. 2009;26:165–72.PubMed Rout R, Mohapatra BN, Kar SK, Ranjit M. Genetic complexity and transmissibility of Plasmodium falciparum parasites causing severe malaria in central-east coast India. Trop Biomed. 2009;26:165–72.PubMed
12.
go back to reference John CC, Park GS, Sam-Agudu N, Opoka RO, Boivin MJ. Elevated serum levels of IL-1ra in children with Plasmodium falciparum malaria are associated with increased severity of disease. Cytokine. 2008;41:204–8.PubMedPubMedCentralCrossRef John CC, Park GS, Sam-Agudu N, Opoka RO, Boivin MJ. Elevated serum levels of IL-1ra in children with Plasmodium falciparum malaria are associated with increased severity of disease. Cytokine. 2008;41:204–8.PubMedPubMedCentralCrossRef
13.
go back to reference Deitsch KW, Chitnis CE. Molecular basis of severe malaria. Proc Natl Acad Sci USA. 2012;109:10130e1.CrossRef Deitsch KW, Chitnis CE. Molecular basis of severe malaria. Proc Natl Acad Sci USA. 2012;109:10130e1.CrossRef
14.
go back to reference Beeson JG, Drew DR, Boyle MJ, Feng G, Fowkes FJI, Richards JS. Merozoite surface proteins in red blood cells, immunity and vaccines against malaria. FEMS Microbiol Rev. 2016;40:343–72.PubMedPubMedCentralCrossRef Beeson JG, Drew DR, Boyle MJ, Feng G, Fowkes FJI, Richards JS. Merozoite surface proteins in red blood cells, immunity and vaccines against malaria. FEMS Microbiol Rev. 2016;40:343–72.PubMedPubMedCentralCrossRef
15.
go back to reference Holder AA, Blackman MJ, Burghaus PA, Chappel JA, Ling IT, McCallum-Deighton N, et al. A malaria merozoite surface protein (MSP1)-structure, processing and function. Mem Inst Oswaldo Cruz. 1992;87(Suppl 3):37–42.PubMedCrossRef Holder AA, Blackman MJ, Burghaus PA, Chappel JA, Ling IT, McCallum-Deighton N, et al. A malaria merozoite surface protein (MSP1)-structure, processing and function. Mem Inst Oswaldo Cruz. 1992;87(Suppl 3):37–42.PubMedCrossRef
16.
go back to reference Hofmann EH, Malafronte RS, Moraes-Avila SL, Osakabe AL, Wunderlich G, Durham AL, et al. Origins of sequence diversity in the malaria vaccine candidate merozoite surface protein -2 (MSP-2) Amazonian of Plasmodium falciparum. Gene. 2006;376:224–30.CrossRef Hofmann EH, Malafronte RS, Moraes-Avila SL, Osakabe AL, Wunderlich G, Durham AL, et al. Origins of sequence diversity in the malaria vaccine candidate merozoite surface protein -2 (MSP-2) Amazonian of Plasmodium falciparum. Gene. 2006;376:224–30.CrossRef
17.
go back to reference Felger I, Irion A, Steiger S, Beck HP. Genotypes of merozoite surface protein 2 of Plasmodium falciparum in Tanzania. Trans R Soc Trop Med Hyg. 1999;93(suppl 1):3–9.PubMedCrossRef Felger I, Irion A, Steiger S, Beck HP. Genotypes of merozoite surface protein 2 of Plasmodium falciparum in Tanzania. Trans R Soc Trop Med Hyg. 1999;93(suppl 1):3–9.PubMedCrossRef
18.
go back to reference Kiwanuka GN. Genetic diversity in Plasmodium falciparum merozoite surface protein 1 and 2 coding genes and its implications in malaria epidemiology: a review of published studies from 1997–2007. J Vector Borne Dis. 2009;46:1–12.PubMed Kiwanuka GN. Genetic diversity in Plasmodium falciparum merozoite surface protein 1 and 2 coding genes and its implications in malaria epidemiology: a review of published studies from 1997–2007. J Vector Borne Dis. 2009;46:1–12.PubMed
19.
go back to reference Ariey F, Hommel D, Le Scanf C, Duchemin JB, Peneau C, Mercereau-Puijalon O. Association of severe malaria with a specific of Plasmodium falciparum genotype in French Guiana. J Inf Dis. 2001;184:237–41.CrossRef Ariey F, Hommel D, Le Scanf C, Duchemin JB, Peneau C, Mercereau-Puijalon O. Association of severe malaria with a specific of Plasmodium falciparum genotype in French Guiana. J Inf Dis. 2001;184:237–41.CrossRef
20.
go back to reference Durand R, Ariey F, Fontanet A, Ranaivo L, Ranarivelo LA, Vonimpaisomihanta JA, et al. Analysis of circulating populations Plasmodium falciparum in mild and severe malaria in two different epidemiological patterns in Madagascar. Trop Med Int Health. 2008;13:1392–9.PubMedCrossRef Durand R, Ariey F, Fontanet A, Ranaivo L, Ranarivelo LA, Vonimpaisomihanta JA, et al. Analysis of circulating populations Plasmodium falciparum in mild and severe malaria in two different epidemiological patterns in Madagascar. Trop Med Int Health. 2008;13:1392–9.PubMedCrossRef
21.
go back to reference Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, Olumese PE, et al. Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Ann Trop Med Parasitol. 2008;102:95–102.PubMedCrossRef Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, Olumese PE, et al. Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Ann Trop Med Parasitol. 2008;102:95–102.PubMedCrossRef
22.
go back to reference Mohammed H, Mindaye T, Belayneh M, Kassa M, Assefa A, Tadesse M, et al. Genetic diversity of Plasmodium falciparum isolates based on MSP-1and MSP-2 genes from Kolla-Shele area, Arbaminch Zuria District, southwest Ethiopia. Malar J. 2015;14:73.PubMedPubMedCentralCrossRef Mohammed H, Mindaye T, Belayneh M, Kassa M, Assefa A, Tadesse M, et al. Genetic diversity of Plasmodium falciparum isolates based on MSP-1and MSP-2 genes from Kolla-Shele area, Arbaminch Zuria District, southwest Ethiopia. Malar J. 2015;14:73.PubMedPubMedCentralCrossRef
23.
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:e0177559.PubMedPubMedCentralCrossRef 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:e0177559.PubMedPubMedCentralCrossRef
24.
go back to reference Mohammed H, Kassa M, Mekete K, Assefa A, Taye G, Commons RJ. Genetic diversity of msp1, msp2 and glurp of Plasmodium falciparum isolates in Northwest Ethiopia. Malar J. 2018;17:386.PubMedPubMedCentralCrossRef Mohammed H, Kassa M, Mekete K, Assefa A, Taye G, Commons RJ. Genetic diversity of msp1, msp2 and glurp of Plasmodium falciparum isolates in Northwest Ethiopia. Malar J. 2018;17:386.PubMedPubMedCentralCrossRef
25.
go back to reference Alelign A, Dejene T. Current status of malaria in Ethiopia; evaluation of the burden, factors for transmission and prevention methods. Acta Parasitol Glob. 2016;7:1–6. Alelign A, Dejene T. Current status of malaria in Ethiopia; evaluation of the burden, factors for transmission and prevention methods. Acta Parasitol Glob. 2016;7:1–6.
26.
go back to reference Aschale Y, Mengist A, Bitew A, Talie A. Prevalence of malaria and associated risk factors among asymptomatic migrant laborers in West Armachiho District, Northwest Ethiopia. Ther Clin Risk Manag. 2018;9:95–101. Aschale Y, Mengist A, Bitew A, Talie A. Prevalence of malaria and associated risk factors among asymptomatic migrant laborers in West Armachiho District, Northwest Ethiopia. Ther Clin Risk Manag. 2018;9:95–101.
27.
go back to reference Federal Ministry of Health (FMoH). National strategy plan for malaria prevention, control and elimination in Ethiopia: 2014–2020. Addis Ababa, Ethiopia; 2014. Federal Ministry of Health (FMoH). National strategy plan for malaria prevention, control and elimination in Ethiopia: 2014–2020. Addis Ababa, Ethiopia; 2014.
28.
go back to reference WHO. Severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000;94:1–18. WHO. Severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000;94:1–18.
29.
go back to reference Federal Ministry of Health of Ethiopia (FMOH). National malaria guidelines. 3rd ed. Addis Ababa: Federal Ministry of Health of Ethiopia (FMOH); 2012. Federal Ministry of Health of Ethiopia (FMOH). National malaria guidelines. 3rd ed. Addis Ababa: Federal Ministry of Health of Ethiopia (FMOH); 2012.
30.
go back to reference WHO. Basic malaria microscopy, Part 1. Learner’s guide. 2nd ed. Geneva: Word Health Organization; 2010. WHO. Basic malaria microscopy, Part 1. Learner’s guide. 2nd ed. Geneva: Word Health Organization; 2010.
31.
go back to reference Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.PubMedCrossRef Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.PubMedCrossRef
32.
go back to reference Vafa M, Troye- Blomberg M, Anchang J, Garcia A, Migot-Nabias F. Multiplicity of Plasmodium falciparum infection in asymptomatic children In Senegal, relation of transmission, age, and erythrocyte variants. Malar J. 2008;9:17.CrossRef Vafa M, Troye- Blomberg M, Anchang J, Garcia A, Migot-Nabias F. Multiplicity of Plasmodium falciparum infection in asymptomatic children In Senegal, relation of transmission, age, and erythrocyte variants. Malar J. 2008;9:17.CrossRef
33.
go back to reference Ntoumi F, Ngoundou-Landji J, Lekoulou F, Luty A, Deloron P, Ringwald P. Site-based study on polymorphism of Plasmodium falciparum msp-1 and msp-2 genes in isolates from two villages in Central Africa. Parassitologia. 2000;42:197–203.PubMed Ntoumi F, Ngoundou-Landji J, Lekoulou F, Luty A, Deloron P, Ringwald P. Site-based study on polymorphism of Plasmodium falciparum msp-1 and msp-2 genes in isolates from two villages in Central Africa. Parassitologia. 2000;42:197–203.PubMed
34.
go back to reference Bouyou-Akotel MK, M’Bondoukwe NP, Mawili-Mboumba DP. Genetic polymorphism of merozoite surface protein-1 in Plasmodium falciparum isolates from patients with mild and severe malaria in Libreville, Gabon. Parasite. 2015;22:12.CrossRef Bouyou-Akotel MK, M’Bondoukwe NP, Mawili-Mboumba DP. Genetic polymorphism of merozoite surface protein-1 in Plasmodium falciparum isolates from patients with mild and severe malaria in Libreville, Gabon. Parasite. 2015;22:12.CrossRef
35.
go back to reference Hamid MAM, Elamin AF, Ali-Albsheer MM, Abdalla AA, Mahgoub NS, Mustafa SO, et al. Multiplicity of infection and genetic diversity of Plasmodium falciparum isolates from patients with uncomplicated and severe malaria in Gezira State, Sudan. Parasit Vectors. 2016;9:362.CrossRef Hamid MAM, Elamin AF, Ali-Albsheer MM, Abdalla AA, Mahgoub NS, Mustafa SO, et al. Multiplicity of infection and genetic diversity of Plasmodium falciparum isolates from patients with uncomplicated and severe malaria in Gezira State, Sudan. Parasit Vectors. 2016;9:362.CrossRef
36.
go back to reference Robert F, Ntoumi F, Angel G, Candito D, Rogier C, Fandeur T, et al. Extensive genetic diversity of Plasmodium falciparum isolates collected from patients with severe malaria in Dakar. Trans R Soc Trop Med Hyg. 1996;90:704–11.PubMedCrossRef Robert F, Ntoumi F, Angel G, Candito D, Rogier C, Fandeur T, et al. Extensive genetic diversity of Plasmodium falciparum isolates collected from patients with severe malaria in Dakar. Trans R Soc Trop Med Hyg. 1996;90:704–11.PubMedCrossRef
37.
go back to reference Hamid MM, 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. Am J Med Sci. 2013;5:95–101.CrossRef Hamid MM, 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. Am J Med Sci. 2013;5:95–101.CrossRef
38.
go back to reference Mayengue PI, Ndounga M, Malonga FV, Bitemo M, Ntoumi F. Genetic polymorphism of merozoite surface protein 1 and merozoite surface protein 2 in Plasmodium falciparum isolates from Brazzaville, Republic of Congo. Malar J. 2011;10:276.PubMedPubMedCentralCrossRef Mayengue PI, Ndounga M, Malonga FV, Bitemo M, Ntoumi F. Genetic polymorphism of merozoite surface protein 1 and merozoite surface protein 2 in Plasmodium falciparum isolates from Brazzaville, Republic of Congo. Malar J. 2011;10:276.PubMedPubMedCentralCrossRef
39.
go back to reference Funwei RI, Thomas BN, Falade CO, Ojurongbe O. Extensive diversity in the allelic frequency of Plasmodium falciparum merozoite surface proteins and glutamate-rich protein in rural and urban settings of southwestern Nigeria. Malar J. 2018;17:1.PubMedPubMedCentralCrossRef Funwei RI, Thomas BN, Falade CO, Ojurongbe O. Extensive diversity in the allelic frequency of Plasmodium falciparum merozoite surface proteins and glutamate-rich protein in rural and urban settings of southwestern Nigeria. Malar J. 2018;17:1.PubMedPubMedCentralCrossRef
40.
41.
go back to reference Oyedeji SI, Awobode HO, Kun J. Limited genetic diversity and low multiplicity of Plasmodium falciparum infection in children with severe malaria in Lafia in North-central Nigeria. J Exp Clin Med. 2013;5:143–7.CrossRef Oyedeji SI, Awobode HO, Kun J. Limited genetic diversity and low multiplicity of Plasmodium falciparum infection in children with severe malaria in Lafia in North-central Nigeria. J Exp Clin Med. 2013;5:143–7.CrossRef
42.
go back to reference Mayeungue PI, Luty AJ, Rogier C, Baragatti M, Kremsner PG, Ntoumi F. The multiplicity of Plasmodium falciparum infections is associated with acquired immunity to asexual blood stage antigens. Microbes Infect. 2009;11:108–14.CrossRef Mayeungue PI, Luty AJ, Rogier C, Baragatti M, Kremsner PG, Ntoumi F. The multiplicity of Plasmodium falciparum infections is associated with acquired immunity to asexual blood stage antigens. Microbes Infect. 2009;11:108–14.CrossRef
43.
go back to reference Smith T, Beck HP, Kitua A, Mwankusye S, Felger I, Fraser-Hurt N, et al. Age dependence of the multiplicity of Plasmodium falciparum infections and other malariological indices in an area of high endemicity. Trans R Soc Med Hyg. 1999;93(Suppl 1):15–20.CrossRef Smith T, Beck HP, Kitua A, Mwankusye S, Felger I, Fraser-Hurt N, et al. Age dependence of the multiplicity of Plasmodium falciparum infections and other malariological indices in an area of high endemicity. Trans R Soc Med Hyg. 1999;93(Suppl 1):15–20.CrossRef
44.
go back to reference Konate L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, et al. 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(Suppl 1):21–8.PubMedCrossRef Konate L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, et al. 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(Suppl 1):21–8.PubMedCrossRef
45.
go back to reference Ogouye’mi-Hounto A, Gazard DK, Ndam N, Topanou E, Garba O, Elegbe P, et al. Genetic polymorphism of merozoite surface protein-1 and merozoite surface protein-2 in Plasmodium falciparum isolates from children in South of Benin. Parasite. 2013;20:37.CrossRef Ogouye’mi-Hounto A, Gazard DK, Ndam N, Topanou E, Garba O, Elegbe P, et al. Genetic polymorphism of merozoite surface protein-1 and merozoite surface protein-2 in Plasmodium falciparum isolates from children in South of Benin. Parasite. 2013;20:37.CrossRef
46.
go back to reference Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, et al. Force of infection is a key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Nat Acad Sci USA. 2012;109:10030–5.PubMedCrossRefPubMedCentral Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, et al. Force of infection is a key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Nat Acad Sci USA. 2012;109:10030–5.PubMedCrossRefPubMedCentral
47.
Metadata
Title
Genetic diversity of Plasmodium falciparum isolates from patients with uncomplicated and severe malaria based on msp-1 and msp-2 genes in Gublak, North West Ethiopia
Authors
Hussein Mohammed
Kedir Hassen
Ashenafi Assefa
Kalkidan Mekete
Gemechu Tadesse
Girum Taye
Robert J. Commons
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/s12936-019-3039-9

Other articles of this Issue 1/2019

Malaria Journal 1/2019 Go to the issue