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1.
World Health Organization, 2014. World Malaria Report 2014. Geneva, Switzerland: World Health Organization.
-
2.
RTS,S Clinical Trials Partnership, 2015. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet 386: 31–45.
-
3.
Mwingira F, Genton B, Kabanywanyi AN, Felger I, 2014. Comparison of detection methods to estimate asexual Plasmodium falciparum parasite prevalence and gametocyte carriage in a community survey in Tanzania. Malar J 13: 433.
-
4.
Kilian AH, Metzger WG, Mutschelknauss EJ, Kabagambe G, Langi P, Korte R, von Sonnenburg F, 2000. Reliability of malaria microscopy in epidemiological studies: results of quality control. Trop Med Int Health 5: 3–8.
-
5.
World Health Organization, 2015. Malaria Rapid Diagnostic Test Performance. Results of WHO Product Testing of Malaria RDTs: Round 6 (2015). Geneva, Switzerland: World Health Organization.
-
6.
Wu L, van den Hoogen LL, Slater H, Walker PG, Ghani AC, Drakeley CJ, Okell LC, 2015. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature 528: S86–S93.
-
7.
Ouedraogo AL, Goncalves BP, Gneme A, Wenger EA, Guelbeogo MW, Ouedraogo A, Gerardin J, Bever CA, Lyons H, Pitroipa X, Verhave JP, Eckhoff PA, Drakeley C, Sauerwein R, Luty AJ, Kouyate B, Bousema T, 2016. Dynamics of the human infectious reservoir for malaria determined by mosquito feeding assays and ultrasensitive malaria diagnosis in Burkina Faso. J Infect Dis 213: 90–99.
-
8.
Lin JT, Ubalee R, Lon C, Balasubramanian S, Kuntawunginn W, Rahman R, Saingam P, Heng TK, Vy D, San S, Nuom S, Burkly H, Chanarat N, Ponsa C, Levitz L, Parobek C, Chuor CM, Somethy S, Spring M, Lanteri C, Gosi P, Meshnick SR, Saunders DL, 2016. Microscopic Plasmodium falciparum gametocytemia and infectivity to mosquitoes in Cambodia. J Infect Dis 213: 1491–1494.
-
9.
Akinyi S, Hayden T, Gamboa D, Torres K, Bendezu J, Abdallah JF, Griffing SM, Quezada WM, Arrospide N, De Oliveira AM, Lucas C, Magill AJ, Bacon DJ, Barnwell JW, Udhayakumar V, 2013. Multiple genetic origins of histidine-rich protein 2 gene deletion in Plasmodium falciparum parasites from Peru. Sci Rep 3: 2797.
-
10.
Pickard AL, Wongsrichanalai C, Purfield A, Kamwendo D, Emery K, Zalewski C, Kawamoto F, Miller RS, Meshnick SR, 2003. Resistance to antimalarials in southeast Asia and genetic polymorphisms in pfmdr1. Antimicrob Agents Chemother 47: 2418–2423.
-
11.
Lefterova MI, Budvytiene I, Sandlund J, Farnert A, Banaei N, 2015. Simple real-time PCR and amplicon sequencing method for identification of Plasmodium species in human whole blood. J Clin Microbiol 53: 2251–2257.
-
12.
Koita OA, Doumbo OK, Ouattara A, Tall LK, Konare A, Diakite M, Diallo M, Sagara I, Masinde GL, Doumbo SN, Dolo A, Tounkara A, Traore I, Krogstad DJ, 2012. False-negative rapid diagnostic tests for malaria and deletion of the histidine-rich repeat region of the hrp2 gene. Am J Trop Med Hyg 86: 194–198.
-
13.
Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I, 2015. Ultra-sensitive detection of Plasmodium falciparum by amplification of multi-copy subtelomeric targets. PLoS Med 12: e1001788.
-
14.
Micallef L, Rodgers P, 2014. eulerAPE: drawing area-proportional 3-venn diagrams using ellipses. PLoS One 9: e101717.
-
15.
Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ, 2012. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun 3: 1237.
-
16.
Walldorf JA, Cohee LM, Coalson JE, Bauleni A, Nkanaunena K, Kapito-Tembo A, Seydel KB, Ali D, Mathanga D, Taylor TE, Valim C, Laufer MK, 2015. School-age children are a reservoir of malaria infection in Malawi. PLoS One 10: e0134061.
-
17.
Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, Lilley K, Krause D, Vallely A, Johnson ML, Gatton ML, Shanks GD, Cheng Q, 2010. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J 9: 254.
-
18.
Abba K, Deeks JJ, Olliaro P, Naing CM, Jackson SM, Takwoingi Y, Donegan S, Garner P, 2011. Rapid diagnostic tests for diagnosing uncomplicated P. falciparum malaria in endemic countries. Cochrane Database Syst Rev CD008122.
-
19.
Iqbal J, Siddique A, Jameel M, Hira PR, 2004. Persistent histidine-rich protein 2, parasite lactate dehydrogenase, and panmalarial antigen reactivity after clearance of Plasmodium falciparum monoinfection. J Clin Microbiol 42: 4237–4241.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 10 | 10 | 3 |
| Full Text Views | 340 | 92 | 0 |
| PDF Downloads | 94 | 16 | 0 |
Estimation of Plasmodium falciparum Transmission Intensity in Lilongwe, Malawi, by Microscopy, Rapid Diagnostic Testing, and Nucleic Acid Detection
Jonathan B. Parr
Jonathan B. Parr
Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina.
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Connor Belson
Connor Belson
Department of Biology, University of North Carolina, Chapel Hill, North Carolina.
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Jaymin C. Patel
Jaymin C. Patel
Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, North Carolina.
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Irving F. Hoffman
Irving F. Hoffman
Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina.
University of North Carolina Project-Malawi, Lilongwe, Malawi.
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Portia Kamthunzi
Portia Kamthunzi
University of North Carolina Project-Malawi, Lilongwe, Malawi.
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Francis Martinson
Francis Martinson
University of North Carolina Project-Malawi, Lilongwe, Malawi.
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Gerald Tegha
Gerald Tegha
University of North Carolina Project-Malawi, Lilongwe, Malawi.
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Isaac Thengolose
Isaac Thengolose
University of North Carolina Project-Malawi, Lilongwe, Malawi.
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Chris Drakeley
Chris Drakeley
London School of Hygiene and Tropical Medicine, London, United Kingdom.
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Steven R. Meshnick
Steven R. Meshnick
Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, North Carolina.
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Veronica Escamillia
Veronica Escamillia
Department of Obstetrics and Gynecology, University of Chicago, Chicago, Illinois.
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Michael Emch
Michael Emch
Department of Geography, University of North Carolina, Chapel Hill, North Carolina.
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Jonathan J. Juliano
Jonathan J. Juliano
Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina.
Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, North Carolina.
Curriculum in Genetics and Molecular Biology, University of North Carolina, Chapel Hill, North Carolina.
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Estimates of malaria transmission intensity (MTI) typically rely upon microscopy or rapid diagnostic testing (RDT). However, these methods are less sensitive than nucleic acid amplification techniques and may underestimate parasite prevalence. We compared microscopy, RDT, and polymerase chain reaction (PCR) for the diagnosis of Plasmodium falciparum parasitemia as part of an MTI study of 800 children and adults conducted in Lilongwe, Malawi. PCR detected more cases of parasitemia than microscopy or RDT. Age less than 5 years predicted parasitemia detected by PCR alone (adjusted odds ratio = 1.61, 95% confidence interval = 1.09–2.38, Wald P = 0.02). In addition, we identified one P. falciparum parasite with a false-negative RDT result due to a suspected deletion of the histidine-rich protein 2 (hrp2) gene and used a novel, ultrasensitive PCR assay to detect low-level parasitemia missed by traditional PCR. Molecular methods should be considered for use in future transmission studies as a supplement to RDT or microscopy.
Author Notes
Financial support: This work was supported by the National Institutes of Allergy and Infectious Diseases (5T32AI007151 to Jonathan B. Parr, 5 T32AI07001–36 to Veronica Escamillia, and R01AI089819 to Jonathan J. Juliano), the UNC Summer Undergraduate Research Gold Fellowship for Connor Belson, a GlaxoSmithKline post-graduate fellowship to Veronica Escamillia, the Population Research Infrastructure Program through funding awarded by the Eunice Kennedy Shriver National Institute of Child Health and Human Development to the Carolina Population Center [R24 HD050924 to Veronica Escamillia], and the National Science Foundation [BCS-1339949 to Michael Emch]. The MTI study was sponsored by GlaxoSmithKline and funded by GlaxoSmithKline and PATH MVI.
Authors' addresses: Jonathan B. Parr and Irving F. Hoffman, Division of Infectious Diseases, University of North Carolina, Chapel Hill, NC, E-mails: jonathan_parr@med.unc.edu and irving_hoffman@med.unc.edu. Connor Belson, Department of Biology, University of North Carolina, Chapel Hill, NC, E-mail: connorbelson@gmail.com. Jaymin C. Patel and Steven R. Meshnick, Department of Epidemiology, Gillings School of Global Public Health, Chapel Hill, NC, E-mails: jaymin86@email.unc.edu and meshnick@email.unc.edu. Portia Kamthunzi, Francis Martinson, Gerald Tegha, and Isaac Thengolose, University of North Carolina Project-Malawi, Lilongwe, Malawi, E-mails: portia@globemw.net, fmartinson@unclilongwe.org, gtegha@unclilongwe.org, and ithengolose@unclilongwe.org. Chris Drakeley, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom, E-mail: chris.drakeley@lshtm.ac.uk. Veronica Escamilla, Center for Infectious Diseases, University of North Carolina, Chapel Hill, NC, and Carolina Population Center, University of North Carolina, Chapel Hill, NC, E-mail: escamill@email.unc.edu. Michael Emch, Department of Geography, University of North Carolina, Chapel Hill, NC, E-mail: emch@med.unc.edu. Jonathan J. Juliano, Division of Infectious Diseases, Department of Medicine, University of North Carolina, Chapel Hill, NC, E-mail: jonathan_juliano@med.unc.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Health Organization, 2014. World Malaria Report 2014. Geneva, Switzerland: World Health Organization.
-
2.
RTS,S Clinical Trials Partnership, 2015. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet 386: 31–45.
-
3.
Mwingira F, Genton B, Kabanywanyi AN, Felger I, 2014. Comparison of detection methods to estimate asexual Plasmodium falciparum parasite prevalence and gametocyte carriage in a community survey in Tanzania. Malar J 13: 433.
-
4.
Kilian AH, Metzger WG, Mutschelknauss EJ, Kabagambe G, Langi P, Korte R, von Sonnenburg F, 2000. Reliability of malaria microscopy in epidemiological studies: results of quality control. Trop Med Int Health 5: 3–8.
-
5.
World Health Organization, 2015. Malaria Rapid Diagnostic Test Performance. Results of WHO Product Testing of Malaria RDTs: Round 6 (2015). Geneva, Switzerland: World Health Organization.
-
6.
Wu L, van den Hoogen LL, Slater H, Walker PG, Ghani AC, Drakeley CJ, Okell LC, 2015. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature 528: S86–S93.
-
7.
Ouedraogo AL, Goncalves BP, Gneme A, Wenger EA, Guelbeogo MW, Ouedraogo A, Gerardin J, Bever CA, Lyons H, Pitroipa X, Verhave JP, Eckhoff PA, Drakeley C, Sauerwein R, Luty AJ, Kouyate B, Bousema T, 2016. Dynamics of the human infectious reservoir for malaria determined by mosquito feeding assays and ultrasensitive malaria diagnosis in Burkina Faso. J Infect Dis 213: 90–99.
-
8.
Lin JT, Ubalee R, Lon C, Balasubramanian S, Kuntawunginn W, Rahman R, Saingam P, Heng TK, Vy D, San S, Nuom S, Burkly H, Chanarat N, Ponsa C, Levitz L, Parobek C, Chuor CM, Somethy S, Spring M, Lanteri C, Gosi P, Meshnick SR, Saunders DL, 2016. Microscopic Plasmodium falciparum gametocytemia and infectivity to mosquitoes in Cambodia. J Infect Dis 213: 1491–1494.
-
9.
Akinyi S, Hayden T, Gamboa D, Torres K, Bendezu J, Abdallah JF, Griffing SM, Quezada WM, Arrospide N, De Oliveira AM, Lucas C, Magill AJ, Bacon DJ, Barnwell JW, Udhayakumar V, 2013. Multiple genetic origins of histidine-rich protein 2 gene deletion in Plasmodium falciparum parasites from Peru. Sci Rep 3: 2797.
-
10.
Pickard AL, Wongsrichanalai C, Purfield A, Kamwendo D, Emery K, Zalewski C, Kawamoto F, Miller RS, Meshnick SR, 2003. Resistance to antimalarials in southeast Asia and genetic polymorphisms in pfmdr1. Antimicrob Agents Chemother 47: 2418–2423.
-
11.
Lefterova MI, Budvytiene I, Sandlund J, Farnert A, Banaei N, 2015. Simple real-time PCR and amplicon sequencing method for identification of Plasmodium species in human whole blood. J Clin Microbiol 53: 2251–2257.
-
12.
Koita OA, Doumbo OK, Ouattara A, Tall LK, Konare A, Diakite M, Diallo M, Sagara I, Masinde GL, Doumbo SN, Dolo A, Tounkara A, Traore I, Krogstad DJ, 2012. False-negative rapid diagnostic tests for malaria and deletion of the histidine-rich repeat region of the hrp2 gene. Am J Trop Med Hyg 86: 194–198.
-
13.
Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I, 2015. Ultra-sensitive detection of Plasmodium falciparum by amplification of multi-copy subtelomeric targets. PLoS Med 12: e1001788.
-
14.
Micallef L, Rodgers P, 2014. eulerAPE: drawing area-proportional 3-venn diagrams using ellipses. PLoS One 9: e101717.
-
15.
Okell LC, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ, 2012. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun 3: 1237.
-
16.
Walldorf JA, Cohee LM, Coalson JE, Bauleni A, Nkanaunena K, Kapito-Tembo A, Seydel KB, Ali D, Mathanga D, Taylor TE, Valim C, Laufer MK, 2015. School-age children are a reservoir of malaria infection in Malawi. PLoS One 10: e0134061.
-
17.
Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, Lilley K, Krause D, Vallely A, Johnson ML, Gatton ML, Shanks GD, Cheng Q, 2010. A large proportion of asymptomatic Plasmodium infections with low and sub-microscopic parasite densities in the low transmission setting of Temotu Province, Solomon Islands: challenges for malaria diagnostics in an elimination setting. Malar J 9: 254.
-
18.
Abba K, Deeks JJ, Olliaro P, Naing CM, Jackson SM, Takwoingi Y, Donegan S, Garner P, 2011. Rapid diagnostic tests for diagnosing uncomplicated P. falciparum malaria in endemic countries. Cochrane Database Syst Rev CD008122.
-
19.
Iqbal J, Siddique A, Jameel M, Hira PR, 2004. Persistent histidine-rich protein 2, parasite lactate dehydrogenase, and panmalarial antigen reactivity after clearance of Plasmodium falciparum monoinfection. J Clin Microbiol 42: 4237–4241.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 10 | 10 | 3 |
| Full Text Views | 340 | 92 | 0 |
| PDF Downloads | 94 | 16 | 0 |