Low parasitemia in submicroscopic infections significantly impacts malaria diagnostic sensitivity in the highlands of Western Kenya

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Lo, Eugenia ^a   Zhou, Guofa ^a   Oo, Winny ^a   Afrane, Yaw ^b   Githeko, Andrew ^b   Yan, Guiyun ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; AGE; ARTICLE; CHILD; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE SEVERITY; DISEASE TRANSMISSION; FALSE NEGATIVE RESULT; GENDER; GENE DOSAGE; HUMAN; INTERMETHOD COMPARISON; KENYA; LIMIT OF DETECTION; MALARIA FALCIPARUM; MICROSCOPY; PARASITE LOAD; POLYMERASE CHAIN REACTION; PREVALENCE; QUANTITATIVE ANALYSIS; SCHOOL CHILD; SENSITIVITY AND SPECIFICITY; ASYMPTOMATIC INFECTIONS; GENETICS; INFANT; MALARIA, FALCIPARUM; PARASITEMIA; PARASITOLOGY; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PROCEDURES;

PROTOZOAL DNA;

ADOLESCENT; ASYMPTOMATIC INFECTIONS; CHILD; CHILD, PRESCHOOL; DNA, PROTOZOAN; HUMANS; INFANT; KENYA; MALARIA, FALCIPARUM; PARASITEMIA; PLASMODIUM FALCIPARUM; POLYMERASE CHAIN REACTION; PREVALENCE; SENSITIVITY AND SPECIFICITY;

EID: 84929497624     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121763     Document Type: Article

References (46)

1. Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malaria J 2012;11:29. doi: 10.1186/1475-2875-11-29 PMID: 22289302
2. Karl S, Gurarie D, Zimmerman PA, King CH, St. Pierre TG, Davis T M E. A sub-microscopic gametocyte reservoir can sustain malaria transmission. PLoS One 2011;6:e20805. doi: 10.1371/journal.pone. 0020805 PMID: 21695129
3. Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis 2009;200:1509-1517. doi: 10. 1086/644781 PMID: 19848588
4. Harris I, Sharrock WW, Bain LM, Gray KA, Bobogare A, Boaz L, et al. 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. Malaria J 2010;9:254. doi: 10.1186/1475-2875-9-254 PMID: 20822506
5. Schachterle SE, Mtove G, Levens JP, Clemens EG, Shi L, Raj A, et al. Prevalence and density-related concordance of three diagnostic tests for malaria in a region of Tanzania with hypoendemic malaria. J Clin Microbiol 2011;49:3885. doi: 10.1128/JCM.01157-11 PMID: 21880972
6. Okell L, Bousema T, Griffin JT, Ouedraogo AL, Ghani AC, Drakeley CJ. Factors determining the occurrence of submicroscopic malaria infections and their relevance for control. Nat Commun 2012;3:1237. doi: 10.1038/ncomms2241 PMID: 23212366
7. Idro R, Aloyo J, Mayende L, Bitarakwate E, John CC, Kivumbi GW. Severe malaria in children in areas with low, moderate and high transmission intensity in Uganda. Trop Med Int Health 2006;11:115-24. PMID: 16398762
8. Okiro EA, Al-Taiar A, Reyburn H, Idro R, Berkley JA, Snow RW. Age patterns of severe paediatric malaria and their relationship to Plasmodium falciparum transmission intensity. Malaria J 2009;8:4.
9. Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, et al. Age-patterns of malaria vary with severity, transmission intensity and seasonality in Sub-Saharan Africa: a systematic review and pooled analysis. PLoS ONE 2010;5:e8988. doi: 10.1371/journal.pone.0008988 PMID: 20126547
10. Munyekenye OG, Githeko AK, Zhou G, Mushinzimana E, Minakawa N, Yan G. Plasmodium falciparum Spatial Analysis, Western Kenya Highlands. Emerg Infect Dis 2005;11:1571-1577. PMID: 16318698
11. Atieli HE, Zhou G, Afrane Y, Lee M-C, Mwanzo I, Githeko AK, et al. Insecticide-treated net (ITN) ownership, usage, and malaria transmission in the highlands of western Kenya. Parasite Vector 2011;4:113. doi: 10.1186/1756-3305-4-113 PMID: 21682919
12. Coleman RE, Sattabongkot J, Promstaporm S, Maneechai N, Tippayachai B, Kengluecha A, et al. Comparison of PCR and microscopy for the detection of asymptomatic malaria in a Plasmodium falciparum/vivax endemic area in Thailand. Malaria J 2006;5:121. PMID: 17169142
13. Gediminas V, Iezhova TA, Kričanauskienč A, Palinauskas V, Sehgal R N M, Bensch S. A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 2005;94:1395-1401.
14. Fancony C, Sebastiao YV, Pires JE, Gamboa D, Nery SV. Performance of microscopy and RDTs in the context of a malaria prevalence survey in Angola: a comparison using PCR as the gold standard. Malaria J 2013;12:284.
15. Khairnar K, Martin D, Lau R, Ralevski F, Pillai DR. Multiples real-time quantitative PCR, microscopy and rapid diagnostic immune-chomatographic tests for the detection of Plasmodium spp: performance, limit of detection analysis and quality assurance. Malaria J 2009;8:284.
16. Pakalapati D, Garg S, Middha S, Kochar A, Subudhi AK, Arunachalam BP, et al. Comparative evaluation of microscopy, OptiMAL (R) and 18S rRNA gene based multiplex PCR for detection of Plasmodium falciparum & Plasmodium vivax from field isolates of Bikaner, India. Asian Pac J Trop Med 2013;6:346-351. doi: 10.1016/S1995-7645 (13) 60037-1 PMID: 23608372
17. Diallo A, Ndam NT, Moussilioous A, Don Santos S, Ndonky A, Borderon M, et al. Asymptomatic carriage of Plasmodium in urban Dakar: the risk of malaria should not be underestimated. PLoS ONE 2012;7:e31100. doi: 10.1371/journal.pone.0031100 PMID: 22363558
18. Bashir IM, Otsyula N, Awinda G, Spring M, Schneider P, Waitumbi JN. Comparison of PfHRP-2/pLDH ELISA, qPCR and microscopy for the detection of Plasmodium events and prediction of sick visits during a malaria vaccine study. PLoS ONE 2013;8:e56828. doi: 10.1371/journal.pone.0056828 PMID: 23554856
19. Shillcutt S, Morel C, Goodman C, Coleman P, Bell D, Whitty C J M, et al. Cost-effectiveness of malaria diagnostic methods in sub-Saharan Africa in an era of combination therapy. Bull World Health Organ 2008;86:2. PMID: 18235877
20. Bejon P, Andrews L, Hunt-Cook A, Sanderson F, Gilbert SC, Hill A V S. Thick blood film examination for Plasmodium falciparum malaria has reduced sensitivity and underestimates parasitaemia. Malaria J 2006;5:104. PMID: 17092336
21. Ochola LB, Vounatsou P, Smith T, Mabaso M L H, Newton C R JC. The reliability of diagnostic techniques in the diagnosis and management of malaria in the absence of a gold standard. Lance Infect Dis 2006;6:582-588. PMID: 16931409
22. Farcas GA, Zhong KJ, Mazzulli T, Kain KC. Evaluation of the RealArt malaria LC real-time PCR assay for malaria diagnosis. J Clin Microbiol 2004;42:636-638. PMID: 14766829
23. Perandin F, Manca N, Calderaro A, Piccolo G, Galati L, Ricci L, et al. Development of a real-time PCR assay for detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for routine clinical diagnosis. J Clin Microbiol 2004;42:1214-1219.
24. Wooden J, Kyes S, Silbley C. PCR and strain identification in Plasmodium falciparum. Parasitol Today 1993;9:303-5. PMID: 15463789
25. Anderson T J C, Su XZ, Bockarie M, Lagog M, Day KP. Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology 1999;119:113-125. PMID: 10466118
26. Rougemont M, Van SM, Sahli R, Hinrikson HP, Bille J, Jaton K. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol 2004;42:5636-5643. PMID: 15583293
27. Jelinek T, Proll S, Hess F, Kabagambe G, Von Sonnenburg E, Loscher T, et al. Geographic differences in the sensitivity of a polymerase chain reaction for the detection of Plasmodium falciparum infection. Am J Trop Med Hyg 1996;55:647-651. PMID: 9025692
28. Minakawa N, Dida GO, Sonye GO, Futami K, Njenga SM. Malaria Vectors in Lake Victoria and Adjacent Habitats in Western Kenya. PLoS ONE 2012;7:e32725. doi: 10.1371/journal.pone.0032725 PMID: 22412913
29. Shanks GD, Hay SI, Omumbo JA, Snow RW. Malaria in Kenya's western highlands. Emerg Infect Dis 2005;11:1425-1432. PMID: 16229773
30. Martens P, Hall L. Malaria on the move: human population movement and malaria transmission. Emerg Infect Dis 2000;6:103-109. PMID: 10756143
31. Ouedraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS One 2009;4:e8410. doi: 10.1371/journal.pone. 0008410 PMID: 20027314
32. Boonma P, Christensen PR, Suwanarusk R, Price RN, Russell B, Lek-Uthai U. Comparison of three molecular methods for the detection and speciation of Plasmodium vivax and Plasmodium falciparum. Malaria J 2007;6:124. PMID: 17868467
33. Morassin B, Fabre R, Berry A, Magnaval JF. One year's experience with the polymerase chain reaction as a routine method for the diagnosis of imported malaria. Am J Trop Med Hyg 2002;66:503-508. PMID: 12201583
34. Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN. 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 1993;58:283-292. PMID: 8479452
35. Manjurano A, Okell L, Lukindo T, Reyburn H, Olomi R, Roper C, et al. Association of sub-microscopic malaria parasite carriage with transmission intensity in northeastern Tanzania. Malaria J 2011;10:370. doi: 10.1186/1475-2875-10-370 PMID: 22177014
36. Rantala AM, Taylor SM, Trottman PA, Luntamo M, Mbewe B, Maleta K, et al. Comparison of real-time PCR and microscopy for malaria parasite detection in Malawian pregnant women. Malaria J 2010;9:269. doi: 10.1186/1475-2875-9-269 PMID: 20925928
37. Mayor A, Moro L, Aguilar R, Bardaji A, Cistero P, Serra-Casas E, et al. How hidden can malaria be in pregnant women? Diagnosis by microscopy, placental histology, polymerase chain reaction and detection of histidine-rich protein 2 in plasma. Clin Infect Dis 2012;54:1561-1568. doi: 10.1093/cid/cis236 PMID: 22447794
38. Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK. Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from Northwest Colombia. Am J Trop Med Hyg 2013;89:178-183. doi: 10.4269/ajtmh.12-0669 PMID: 23716408
39. Kaisar M M M, Supali T, Wiria AE, Hamid F, Wammes LJ, Sartono E, et al. Epidemiology of Plasmodium infections in Flores Island, Indonesia using real-time PCR. Malaria J 2013;12:169. doi: 10.1186/1475-2875-12-169 PMID: 23706132
40. Ohrt C, Sutamihardja MA, Tang D, Kain KC. Impact of microscopy error on estimates of protective efficacy in malaria-prevention trials. J Infect Dis 2002;186:540-546. PMID: 12195382
41. Perandin F, Manca N, Calderaro A, Piccolo G, Galati L, Ricci L, et al. Development of a real-time PCR assay for detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for routine clinical diagnosis. J Clin Microviol 2004;42:1214-9. PMID: 15004078
42. Boonma P, Christensen PR, Suwanarusk R, Price RN, Russell B, Lek-Uthai U. Comparison of three molecular methods for the detection and speciation of Plasmodium vivax and Plasmodium falciparum. Malaria J 2007;6:124. PMID: 17868467
43. Mens P, Spieker N, Omar S, Heijnen M, Schallig H, Kager PA. Is molecular biology the best alternative for diagnosis of malaria to microscopy? A comparison between microscopy, antigen detection and molecular tests in rural Kenya and Urban Tanzania. Trop Med Int Health 2007;12:238-244. PMID: 17300631
44. O'Meara W, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. Effect of a fall in malaria transmission on morbidity and mortality on Kilifi, Kenya. The Lancet 2008;372:1555-1562. doi: 10.1016/S0140-6736 (08) 61655-4 PMID: 18984188
45. Greenwood B. Review: Intermittent preventive treatment-a new approach to the prevention of malaria in children in areas with seasonal malaria transmission. Trop Med Int Health 2008;11:983-91.
46. Grobusch MP, Leli B, Schwarz NG, Gabor J, Dornemann J, Potschke M, et al. Intermittent preventive treatment against malaria in infeants in Gabon-a randomized, double-blind, placebo-controlled trial. J Infect Dis 2007;196:1595-602. PMID: 18008242