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Zotero
EndNote
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Das S et al. 2017. Performance of a high-sensitivity rapid diagnostic test for Plasmodium falciparum malaria in asymptomatic individuals from Uganda and Myanmar and naive human challenge infections. Am J Trop Med Hyg 97: 1540–1550.
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Aydin-Schmidt B, Xu W, Gonzalez IJ, Polley SD, Bell D, Shakely D, Msellem MI, Björkman A, Mårtensson A, 2014. Loop mediated isothermal amplification (LAMP) accurately detects malaria DNA from filter paper blood samples of low density parasitaemias. PLoS One 9: e103905.
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Cook J et al. 2015. Loop-mediated isothermal amplification (LAMP) for point-of-care detection of asymptomatic low-density malaria parasite carriers in Zanzibar. Malar J 14: 43.
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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.
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Direct Estimation of Sensitivity of Plasmodium falciparum Rapid Diagnostic Test for Active Case Detection in a High-Transmission Community Setting
Steve M. Taylor
Steve M. Taylor
Division of Infectious Diseases, Duke University Medical Center, Durham, North Carolina;
Duke Global Health Institute, Durham, North Carolina;
Department of Epidemiology, University of North Carolina Gillings School of Global Public Health, Chapel Hill, North Carolina;
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Duke Global Health Institute, Durham, North Carolina;
Department of Epidemiology, University of North Carolina Gillings School of Global Public Health, Chapel Hill, North Carolina;
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Kelsey M. Sumner
Kelsey M. Sumner
Division of Infectious Diseases, Duke University Medical Center, Durham, North Carolina;
Department of Epidemiology, University of North Carolina Gillings School of Global Public Health, Chapel Hill, North Carolina;
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Department of Epidemiology, University of North Carolina Gillings School of Global Public Health, Chapel Hill, North Carolina;
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Betsy Freedman
Betsy Freedman
Division of Infectious Diseases, Duke University Medical Center, Durham, North Carolina;
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Judith N. Mangeni
Judith N. Mangeni
College of Health Sciences, Moi University, Eldoret, Kenya
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Andrew A. Obala
Andrew A. Obala
College of Health Sciences, Moi University, Eldoret, Kenya
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Wendy Prudhomme O’Meara
Wendy Prudhomme O’Meara
Division of Infectious Diseases, Duke University Medical Center, Durham, North Carolina;
Duke Global Health Institute, Durham, North Carolina;
College of Health Sciences, Moi University, Eldoret, Kenya
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Duke Global Health Institute, Durham, North Carolina;
College of Health Sciences, Moi University, Eldoret, Kenya
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Community-based active case detection of malaria parasites with conventional rapid diagnostic tests (cRDTs) is a strategy used most commonly in low-transmission settings. We estimated the sensitivity of this approach in a high-transmission setting in Western Kenya. We tested 3,547 members of 912 households identified in 2013–2014 by index children with (case) and without (control) cRDT-positive malaria. All were tested for Plasmodium falciparum with both a cRDT targeting histidine-rich protein 2 and with an ultrasensitive real-time polymerase chain reaction (PCR). We computed cRDT sensitivity against PCR as the referent, compared prevalence between participant types, and estimated cRDT detectability as a function of PCR-estimated parasite density. Parasite prevalence was 22.9% by cRDTs and 61.5% by PCR. Compared with children aged < 5 years or adults aged > 15 years, geometric mean parasite densities (95% CI) were highest in school-age children aged 5–15 years (8.4 p/uL; 6.6–10.6). The overall sensitivity of cRDT was 36%; among asymptomatic household members, cRDT sensitivity was 25.5% and lowest in adults aged > 15 years (15.8%). When modeled as a function of parasite density, relative to school-age children, the probability of cRDT positivity was reduced in both children aged < 5 years (odds ratio [OR] 0.48; 95% CI: 0.34–0.69) and in adults aged > 15 years (OR: 0.35; 95% CI: 0.27–0.47). An HRP2-detecting cRDT had poor sensitivity for active P. falciparum case detection in asymptomatic community members, and sensitivity was lowest in highly prevalent low-density infections and in adults. Future studies can model the incremental effects of high-sensitivity rapid diagnostic tests and the impacts on transmission.
- Supplemental Materials (MS Word 77 KB)
Author Notes
Financial support: This work was supported by the Malaria Eradication Scientific Alliance (no grant number) to W. P. O. and the National Institute for Allergy and Infectious Diseases at the National Institutes of Health (grant number R03AI146406) to S. M. T.
Authors’ addresses: Steve M. Taylor, Betsy Freedman, and Wendy Prudhomme O’Meara, Duke University, Durham, NC, E-mails: steve.taylor@duke.edu, betsy.freedman@duke.edu, and wendy.omeara@duke.edu. Kelsey M. Sumner, University of North Carolina at Chapel Hill, Chapel Hill, NC, E-mail: kelseyms@live.unc.edu. Judith N. Mangeni and Andrew A. Obala, Moi University, Eldoret, Kenya, E-mails: jmangeni@cartafrica.org and andrew.obala@gmail.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Bhatt S et al. 2015. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526: 207–211.
-
2.
Gething PW et al. 2016. Mapping Plasmodium falciparum mortality in Africa between 1990 and 2015. N Engl J Med 375: 2435–2445.
-
3.
Sturrock HJ, Hsiang MS, Cohen JM, Smith DL, Greenhouse B, Bousema T, Gosling RD, 2013. Targeting asymptomatic malaria infections: active surveillance in control and elimination. PLoS Med 10: e1001467.
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4.
WHO, 2017. A Framework for Malaria Elimination. Available at: http://www.who.int/malaria/publications/atoz/9789241511988/en/. Accessed October 8, 2018.
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5.
Smith Gueye C et al. 2013. Active case detection for malaria elimination: a survey among Asia Pacific countries. Malar J 12: 358.
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6.
Larsen DA, Winters A, Cheelo S, Hamainza B, Kamuliwo M, Miller JM, Bridges DJ, 2017. Shifting the burden or expanding access to care? Assessing malaria trends following scale-up of community health worker malaria case management and reactive case detection. Malar J 16: 441.
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7.
Pinchoff J, Henostroza G, Carter BS, Roberts ST, Hatwiinda S, Hamainza B, Hawela M, Curriero FC, 2015. Spatial patterns of incident malaria cases and their household contacts in a single clinic catchment area of Chongwe district, Zambia. Malar J 14: 305.
-
8.
Chihanga S, Haque U, Chanda E, Mosweunyane T, Moakofhi K, Jibril HB, Motlaleng M, Zhang W, Glass GE, 2016. Malaria elimination in Botswana, 2012–2014: achievements and challenges. Parasit Vectors 9: 99.
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9.
Deutsch-Feldman M et al. 2018. Efficiency of a malaria reactive test-and-treat program in southern Zambia: a prospective, observational study. Am J Trop Med Hyg 98: 1382–1388.
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10.
Littrell M, Sow GD, Ngom A, Ba M, Mboup BM, Dieye Y, Mutombo B, Earle D, Steketee RW, 2013. Case investigation and reactive case detection for malaria elimination in northern Senegal. Malar J 12: 331.
-
11.
Sturrock HJ, Novotny JM, Kunene S, Dlamini S, Zulu Z, Cohen JM, Hsiang MS, Greenhouse B, Gosling RD, 2013. Reactive case detection for malaria elimination: real-life experience from an ongoing program in Swaziland. PLoS One 8: e63830.
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12.
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13.
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-
14.
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 7: CD008122.
-
15.
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.
-
16.
Mogeni P et al. 2017. Detecting malaria hotspots: a comparison of rapid diagnostic test, microscopy, and polymerase chain reaction. J Infect Dis 216: 1091–1098.
-
17.
Cook J et al. 2015. Mass screening and treatment on the basis of results of a Plasmodium falciparum-specific rapid diagnostic test did not reduce malaria incidence in Zanzibar. J Infect Dis 211: 1476–1483.
-
18.
WHO, 2017. Malaria Rapid Diagnostic Test Performance. Results of WHO Product Testing of Malaria RDTs: Round 7 (2015–2016). Available at: http://www.who.int/malaria/publications/atoz/978924151268/en/. Accessed October 10, 2018.
-
19.
Das S et al. 2017. Performance of a high-sensitivity rapid diagnostic test for Plasmodium falciparum malaria in asymptomatic individuals from Uganda and Myanmar and naive human challenge infections. Am J Trop Med Hyg 97: 1540–1550.
-
20.
Aydin-Schmidt B, Xu W, Gonzalez IJ, Polley SD, Bell D, Shakely D, Msellem MI, Björkman A, Mårtensson A, 2014. Loop mediated isothermal amplification (LAMP) accurately detects malaria DNA from filter paper blood samples of low density parasitaemias. PLoS One 9: e103905.
-
21.
Cook J et al. 2015. Loop-mediated isothermal amplification (LAMP) for point-of-care detection of asymptomatic low-density malaria parasite carriers in Zanzibar. Malar J 14: 43.
-
22.
Hofmann NE et al. 2018. Assessment of ultra-sensitive malaria diagnosis versus standard molecular diagnostics for malaria elimination: an in-depth molecular community cross-sectional study. Lancet Infect Dis 18: 1108–1116.
-
23.
Obala AA, Mangeni JN, Platt A, Aswa D, Abel L, Namae J, Prudhomme O’Meara W, 2015. What is threatening the effectiveness of insecticide-treated bednets? A case-control study of environmental, behavioral, and physical factors associated with prevention failure. PLoS One 10: e0132778.
-
24.
Demas A et al. 2011. Applied genomics: data mining reveals species-specific malaria diagnostic targets more sensitive than 18S rRNA. J Clin Microbiol 49: 2411–2418.
-
25.
Beshir KB, Hallett RL, Eziefula AC, Bailey R, Watson J, Wright SG, Chiodini PL, Polley SD, Sutherland CJ, 2010. Measuring the efficacy of anti-malarial drugs in vivo: quantitative PCR measurement of parasite clearance. Malar J 9: 312.
-
26.
Thompson JD, Higgins DG, Gibson TJ, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
-
27.
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.
-
28.
Rantala AM, Taylor SM, Trottman PA, Luntamo M, Mbewe B, Maleta K, Kulmala T, Ashorn P, Meshnick SR, 2010. Comparison of real-time PCR and microscopy for malaria parasite detection in Malawian pregnant women. Malar J 9: 269.
-
29.
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.
-
30.
Girma S, Cheaveau J, Mohon AN, Marasinghe D, Legese R, Balasingam N, Abera A, Feleke SM, Golassa L, Pillai DR, 2019. Prevalence and epidemiological characteristics of asymptomatic malaria based on ultrasensitive diagnostics: a cross-sectional study. Clin Infect Dis 69: 1003.
-
31.
Beshir KB, Sepulveda N, Bharmal J, Robinson A, Mwanguzi J, Busula AO, de Boer JG, Sutherland C, Cunningham J, Hopkins H, 2017. Plasmodium falciparum parasites with histidine-rich protein 2 (pfhrp2) and pfhrp3 gene deletions in two endemic regions of Kenya. Sci Rep 7: 14718.
-
32.
Levitt B, Obala A, Langdon S, Corcoran D, O’Meara WP, Taylor SM, 2017. Overlap extension barcoding for the next generation sequencing and genotyping of Plasmodium falciparum in individual patients in western Kenya. Sci Rep 7: 41108.
-
33.
Dalrymple U, Arambepola R, Gething PW, Cameron E, 2018. How long do rapid diagnostic tests remain positive after anti-malarial treatment? Malar J 17: 228.
-
34.
Markwalter CF, Mudenda L, Leelawong M, Kimmel DW, Nourani A, Mbambara S, Thuma PE, Wright DW, 2018. Evidence for histidine-rich protein 2 immune complex formation in symptomatic patients in southern Zambia. Malar J 17: 256.
-
35.
Taylor DW, Bobbili N, Khadka VS, Quakyi IA, Leke RG, 2017. Individuals living in a malaria-endemic area of Cameroon do not have an acquired antibody response to Plasmodium falciparum histidine-rich protein 2. Malar J 16: 58.
-
36.
Das S, Peck RB, Barney R, Jang IK, Kahn M, Zhu M, Domingo GJ, 2018. Performance of an ultra-sensitive Plasmodium falciparum HRP2-based rapid diagnostic test with recombinant HRP2, culture parasites, and archived whole blood samples. Malar J 17: 118.
-
37.
Imwong M, Hanchana S, Malleret B, Rénia L, Day NP, Dondorp A, Nosten F, Snounou G, White NJ, 2014. High-throughput ultrasensitive molecular techniques for quantifying low-density malaria parasitemias. J Clin Microbiol 52: 3303–3309.
-
38.
Cheng Z, Wang D, Tian X, Sun Y, Sun X, Xiao N, Zheng Z, 2015. Capture and ligation probe-PCR (CLIP-PCR) for molecular screening, with application to active malaria surveillance for elimination. Clin Chem 61: 821–828.
-
39.
Lucchi NW, Narayanan J, Karell MA, Xayavong M, Kariuki S, DaSilva AJ, Hill V, Udhayakumar V, 2013. Molecular diagnosis of malaria by photo-induced electron transfer fluorogenic primers: PET-PCR. PLoS One 8: e56677.
-
40.
Goncalves BP et al. 2017. Examining the human infectious reservoir for Plasmodium falciparum malaria in areas of differing transmission intensity. Nat Commun 8: 1133.
-
41.
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.
-
42.
Slater HC et al. 2019. The temporal dynamics and infectiousness of subpatent Plasmodium falciparum infections in relation to parasite density. Nat Commun 10: 1433.
-
43.
Landier J et al. 2018. Operational performance of a Plasmodium falciparum ultrasensitive rapid diagnostic test for detection of asymptomatic infections in eastern Myanmar. J Clin Microbiol 56: e00565.
-
44.
Murphy SC et al. 2012. Real-time quantitative reverse transcription PCR for monitoring of blood-stage Plasmodium falciparum infections in malaria human challenge trials. Am J Trop Med Hyg 86: 383–394.
-
45.
Lawpoolsri S, Chavez IF, Yimsamran S, Puangsa-Art S, Thanyavanich N, Maneeboonyang W, Chaimungkun W, Singhasivanon P, Maguire JH, Hungerford LL, 2010. The impact of human reservoir of malaria at a community-level on individual malaria occurrence in a low malaria transmission setting along the Thai-Myanmar border. Malar J 9: 143.
-
46.
Stresman GH, Kamanga A, Moono P, Hamapumbu H, Mharakurwa S, Kobayashi T, Moss WJ, Shiff C, 2010. A method of active case detection to target reservoirs of asymptomatic malaria and gametocyte carriers in a rural area in southern province, Zambia. Malar J 9: 265.
-
47.
Smith JL, Auala J, Tambo M, Haindongo E, Katokele S, Uusiku P, Gosling R, Kleinschmidt I, Mumbengegwi D, Sturrock HJW, 2017. Spatial clustering of patent and sub-patent malaria infections in northern Namibia: implications for surveillance and response strategies for elimination. PLoS One 12: e0180845.
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