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-
1.
White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM, 2014. Malaria. Lancet 383: 723–735.
-
2.
Howes RE et al.., 2011. The global distribution of the Duffy blood group. Nat Commun 2: 266.
-
3.
Howes RE et al.., 2015. Plasmodium vivax transmission in Africa. PLoS Negl Trop Dis 9: e0004222.
-
4.
Mouatcho JC, Goldring JP, 2013. Malaria rapid diagnostic tests: challenges and prospects. J Med Microbiol 62: 1491–1505.
-
5.
World Health Organization, 2015. Guidelines for the Treatment of Malaria. Geneva, Switzerland: WHO.
-
6.
Mueller I, Zimmerman PA, Reeder JC, 2007. Plasmodium malariae and Plasmodium ovale–the “bashful” malaria parasites. Trends Parasitol 23: 278–283.
-
7.
Boudin C, Robert V, Verhave JP, Carnevale P, Ambroise-Thomas P, 1991. Plasmodium falciparum and P. malariae epidemiology in a West African village. Bull World Health Organ 69: 199–205.
-
8.
Barnish G, Maude GH, Bockarie MJ, Eggelte TA, Greenwood BM, 1993. The epidemiology of malaria in southern Sierra Leone. Parassitologia 35 (Suppl ):1–4.
-
9.
Trape JF et al.., 1994. The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am J Trop Med Hyg 51: 123–137.
-
10.
Browne EN, Frimpong E, Sievertsen J, Hagen J, Hamelmann C, Dietz K, Horstmann RD, Burchard GD, 2000. Malariometric update for the rainforest and savanna of Ashanti region, Ghana. Ann Trop Med Parasitol 94: 15–22.
-
11.
Bonnet S, Paul RE, Gouagna C, Safeukui I, Meunier JY, Gounoue R, Boudin C, 2002. Level and dynamics of malaria transmission and morbidity in an equatorial area of South Cameroon. Trop Med Int Health 7: 249–256.
-
12.
Doderer-Lang C et al.., 2014. The ears of the African elephant: unexpected high seroprevalence of Plasmodium ovale and Plasmodium malariae in healthy populations in Western Africa. Malar J 13: 240.
-
13.
Amanfo SA, Mduluza T, Midzi N, Cavanagh DR, Mutapi F, 2016. Seroepidemiology of Plasmodium species infections in Zimbabwean population. Malar J 15: 267.
-
14.
Sitali L, Chipeta J, Miller JM, Moonga HB, Kumar N, Moss WJ, Michelo C, 2015. Patterns of mixed Plasmodium species infections among children six years and under in selected malaria hyper-endemic communities of Zambia: population-based survey observations. BMC Infect Dis 15: 204.
-
15.
Lo E, Nguyen K, Nguyen J, Hemming-Schroeder E, Xu J, Etemesi H, Githeko A, Yan G, 2017. Plasmodium malariae prevalence and csp gene diversity, Kenya, 2014 and 2015. Emerg Infect Dis 23: 601–610.
-
16.
Clark TD, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C, Greenhouse B, Staedke SG, Kamya MR, Dorsey G, Rosenthal PJ, 2010. Incidence of malaria and efficacy of combination antimalarial therapies over 4 years in an urban cohort of Ugandan children. PLoS One 5: e11759.
-
17.
Betson M, Sousa-Figueiredo JC, Atuhaire A, Arinaitwe M, Adriko M, Mwesigwa G, Nabonge J, Kabatereine NB, Sutherland CJ, Stothard JR, 2014. Detection of persistent Plasmodium spp. infections in Ugandan children after artemether-lumefantrine treatment. Parasitology 141: 1880–1890.
-
18.
Yeka A et al.., 2012. Malaria in Uganda: challenges to control on the long road to elimination: I. Epidemiology and current control efforts. Acta Trop 121: 184–195.
-
19.
Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE, 1995. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg 52: 565–568.
-
20.
Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN, 1993. Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol 58: 283–292.
-
21.
Nsobya SL, Parikh S, Kironde F, Lubega G, Kamya MR, Rosenthal PJ, Dorsey G, 2004. Molecular evaluation of the natural history of asymptomatic parasitemia in Ugandan children. J Infect Dis 189: 2220–2226.
-
22.
Katureebe A et al.., 2016. Measures of malaria burden after long-lasting insecticidal net distribution and indoor residual spraying at three sites in Uganda: a prospective observational study. PLoS Med 13: e1002167.
-
23.
Raouf S et al.., 2017. Resurgence of malaria following discontinuation of indoor residual spraying of insecticide in a previously high transmission intensity area of Uganda. Clin Infect Dis 65: 453–460.
-
24.
Poirier P et al.., 2016. The hide and seek of Plasmodium vivax in West Africa: report from a large-scale study in Beninese asymptomatic subjects. Malar J 15: 570.
-
25.
Rogier E, Moss DM, Chard AN, Trinies V, Doumbia S, Freeman MC, Lammie PJ, 2017. Evaluation of immunoglobulin G responses to Plasmodium falciparum and Plasmodium vivax in Malian school children using multiplex bead assay. Am J Trop Med Hyg 96: 312–318.
-
26.
Calleri G, Balbiano R, Caramello P, 2013. Are artemisinin-based combination therapies effective against Plasmodium malariae? J Antimicrob Chemother 68: 1447–1448.
-
27.
Roh ME, Oyet C, Orikiriza P, Wade M, Kiwanuka GN, Mwanga-Amumpaire J, Parikh S, Boum Y, 2016. Asymptomatic Plasmodium infections in children in low malaria transmission setting, southwestern Uganda. Emerg Infect Dis 22: 1494–1498.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1013 | 683 | 255 |
| Full Text Views | 713 | 23 | 3 |
| PDF Downloads | 287 | 25 | 3 |
Plasmodium Species Infecting Children Presenting with Malaria in Uganda
Victor Asua
Victor Asua
Infectious Diseases Research Collaboration, Kampala, Uganda;
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Stephen Tukwasibwe
Stephen Tukwasibwe
Infectious Diseases Research Collaboration, Kampala, Uganda;
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Melissa Conrad
Melissa Conrad
Department of Medicine, University of California, San Francisco, San Francisco, California; Department of Medicine, Makerere University, Kampala, Uganda;
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Andrew Walakira
Andrew Walakira
Infectious Diseases Research Collaboration, Kampala, Uganda;
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Joaniter I. Nankabirwa
Joaniter I. Nankabirwa
Infectious Diseases Research Collaboration, Kampala, Uganda;
Deparment of Pathology, Makerere University, Kampala, Uganda
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Deparment of Pathology, Makerere University, Kampala, Uganda
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Levicatus Mugenyi
Levicatus Mugenyi
Infectious Diseases Research Collaboration, Kampala, Uganda;
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Moses R. Kamya
Moses R. Kamya
Infectious Diseases Research Collaboration, Kampala, Uganda;
Deparment of Pathology, Makerere University, Kampala, Uganda
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Deparment of Pathology, Makerere University, Kampala, Uganda
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Samuel L. Nsobya
Samuel L. Nsobya
Infectious Diseases Research Collaboration, Kampala, Uganda;
Deparment of Pathology, Makerere University, Kampala, Uganda
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Deparment of Pathology, Makerere University, Kampala, Uganda
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Philip J. Rosenthal
Philip J. Rosenthal
Department of Medicine, University of California, San Francisco, San Francisco, California; Department of Medicine, Makerere University, Kampala, Uganda;
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Contributions of species other than Plasmodium falciparum to human malaria in sub-Saharan Africa are uncertain. We collected blood from children aged 6 months to 10 years diagnosed with malaria by Giemsa-stained blood smears (176 subjects) or histidine rich protein-2-based rapid diagnostic tests (323 subjects) in 2016; 50 samples from each of 10 sites across Uganda were studied to identify infecting species. Of 499 available samples, 474 demonstrated plasmodial infection by polymerase chain reaction amplification of 18S ribosomal RNA genes, including P. falciparum in 472, Plasmodium malariae in 22, Plasmodium ovale in 15, and Plasmodium vivax in four; 435 were pure P. falciparum, two did not contain P. falciparum, and the remainder were mixed infections including P. falciparum. The prevalence of nonfalciparum species varied geographically. Stratifying based on recent history of indoor residual spraying (IRS) of insecticides, nonfalciparum infections were seen in 27/189 (14.8%) samples from sites that received and 13/285 (4.6%) samples from sites that did not receive IRS since 2010 (P = 0.0013). Overall, 39/474 (8.2%) samples from individuals diagnosed with malaria included nonfalciparum infections. Thus, a substantial proportion of episodes of malaria in Uganda include infections with plasmodial species other than P. falciparum.
Author Notes
Authors’ addresses: Victor Asua, Stephen Tukwasibwe, and Andrew Walakira, Laboratory Unit, Infectious Diseases Research Collaboration, Kampala, Uganda, E-mails: victorasua@yahoo.co.uk, stephentukwasibwe@yahoo.com, and w.andrew01@yahoo.com. Melissa Conrad and Philip J. Rosenthal, Department of Medicine, University of California, San Francisco, Medicine, San Francisco, CA, E-mails: melissa.conrad@ucsf.edu and philip.rosenthal@ucsf.edu. Joaniter I. Nankabirwa, Department of Medicine, Makerere University College of Health Sciences, Kampala, Uganda, and Infectious Disease Research Collaboration, Kampala, Uganda, E-mail: jnankabirwa@yahoo.co.uk. Levicatus Mugenyi, Infectious Diseases Research Collaboration, Kampala, Uganda, and Universiteit Hasselt, I-Biostat, Diepenbeek, Belgium, E-mail: lmugenyi005@gmail.com. Moses R. Kamya, Department of Medicine, Makerere University College of Health Science, Kampala, Uganda, E-mail: mkamya@idrc-uganda.org. Samuel L. Nsobya, Laboratory Unit, Uganda Malaria Surveillance Program, Kampala, Uganda, E-mail: samnsobya@yahoo.co.uk.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM, 2014. Malaria. Lancet 383: 723–735.
-
2.
Howes RE et al.., 2011. The global distribution of the Duffy blood group. Nat Commun 2: 266.
-
3.
Howes RE et al.., 2015. Plasmodium vivax transmission in Africa. PLoS Negl Trop Dis 9: e0004222.
-
4.
Mouatcho JC, Goldring JP, 2013. Malaria rapid diagnostic tests: challenges and prospects. J Med Microbiol 62: 1491–1505.
-
5.
World Health Organization, 2015. Guidelines for the Treatment of Malaria. Geneva, Switzerland: WHO.
-
6.
Mueller I, Zimmerman PA, Reeder JC, 2007. Plasmodium malariae and Plasmodium ovale–the “bashful” malaria parasites. Trends Parasitol 23: 278–283.
-
7.
Boudin C, Robert V, Verhave JP, Carnevale P, Ambroise-Thomas P, 1991. Plasmodium falciparum and P. malariae epidemiology in a West African village. Bull World Health Organ 69: 199–205.
-
8.
Barnish G, Maude GH, Bockarie MJ, Eggelte TA, Greenwood BM, 1993. The epidemiology of malaria in southern Sierra Leone. Parassitologia 35 (Suppl ):1–4.
-
9.
Trape JF et al.., 1994. The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am J Trop Med Hyg 51: 123–137.
-
10.
Browne EN, Frimpong E, Sievertsen J, Hagen J, Hamelmann C, Dietz K, Horstmann RD, Burchard GD, 2000. Malariometric update for the rainforest and savanna of Ashanti region, Ghana. Ann Trop Med Parasitol 94: 15–22.
-
11.
Bonnet S, Paul RE, Gouagna C, Safeukui I, Meunier JY, Gounoue R, Boudin C, 2002. Level and dynamics of malaria transmission and morbidity in an equatorial area of South Cameroon. Trop Med Int Health 7: 249–256.
-
12.
Doderer-Lang C et al.., 2014. The ears of the African elephant: unexpected high seroprevalence of Plasmodium ovale and Plasmodium malariae in healthy populations in Western Africa. Malar J 13: 240.
-
13.
Amanfo SA, Mduluza T, Midzi N, Cavanagh DR, Mutapi F, 2016. Seroepidemiology of Plasmodium species infections in Zimbabwean population. Malar J 15: 267.
-
14.
Sitali L, Chipeta J, Miller JM, Moonga HB, Kumar N, Moss WJ, Michelo C, 2015. Patterns of mixed Plasmodium species infections among children six years and under in selected malaria hyper-endemic communities of Zambia: population-based survey observations. BMC Infect Dis 15: 204.
-
15.
Lo E, Nguyen K, Nguyen J, Hemming-Schroeder E, Xu J, Etemesi H, Githeko A, Yan G, 2017. Plasmodium malariae prevalence and csp gene diversity, Kenya, 2014 and 2015. Emerg Infect Dis 23: 601–610.
-
16.
Clark TD, Njama-Meya D, Nzarubara B, Maiteki-Sebuguzi C, Greenhouse B, Staedke SG, Kamya MR, Dorsey G, Rosenthal PJ, 2010. Incidence of malaria and efficacy of combination antimalarial therapies over 4 years in an urban cohort of Ugandan children. PLoS One 5: e11759.
-
17.
Betson M, Sousa-Figueiredo JC, Atuhaire A, Arinaitwe M, Adriko M, Mwesigwa G, Nabonge J, Kabatereine NB, Sutherland CJ, Stothard JR, 2014. Detection of persistent Plasmodium spp. infections in Ugandan children after artemether-lumefantrine treatment. Parasitology 141: 1880–1890.
-
18.
Yeka A et al.., 2012. Malaria in Uganda: challenges to control on the long road to elimination: I. Epidemiology and current control efforts. Acta Trop 121: 184–195.
-
19.
Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE, 1995. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg 52: 565–568.
-
20.
Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN, 1993. Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol 58: 283–292.
-
21.
Nsobya SL, Parikh S, Kironde F, Lubega G, Kamya MR, Rosenthal PJ, Dorsey G, 2004. Molecular evaluation of the natural history of asymptomatic parasitemia in Ugandan children. J Infect Dis 189: 2220–2226.
-
22.
Katureebe A et al.., 2016. Measures of malaria burden after long-lasting insecticidal net distribution and indoor residual spraying at three sites in Uganda: a prospective observational study. PLoS Med 13: e1002167.
-
23.
Raouf S et al.., 2017. Resurgence of malaria following discontinuation of indoor residual spraying of insecticide in a previously high transmission intensity area of Uganda. Clin Infect Dis 65: 453–460.
-
24.
Poirier P et al.., 2016. The hide and seek of Plasmodium vivax in West Africa: report from a large-scale study in Beninese asymptomatic subjects. Malar J 15: 570.
-
25.
Rogier E, Moss DM, Chard AN, Trinies V, Doumbia S, Freeman MC, Lammie PJ, 2017. Evaluation of immunoglobulin G responses to Plasmodium falciparum and Plasmodium vivax in Malian school children using multiplex bead assay. Am J Trop Med Hyg 96: 312–318.
-
26.
Calleri G, Balbiano R, Caramello P, 2013. Are artemisinin-based combination therapies effective against Plasmodium malariae? J Antimicrob Chemother 68: 1447–1448.
-
27.
Roh ME, Oyet C, Orikiriza P, Wade M, Kiwanuka GN, Mwanga-Amumpaire J, Parikh S, Boum Y, 2016. Asymptomatic Plasmodium infections in children in low malaria transmission setting, southwestern Uganda. Emerg Infect Dis 22: 1494–1498.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1013 | 683 | 255 |
| Full Text Views | 713 | 23 | 3 |
| PDF Downloads | 287 | 25 | 3 |