Colorimetric tests for diagnosis of filarial infection and vector surveillance using noninstrumented Nucleic acid loop-mediated isothermal amplification (NINA-LAMP)

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Poole, Catherine B ^a   Li, Zhiru ^a   Alhassan, Andy ^a   Guelig, Dylan ^b   Diesburg, Steven ^b   Tanner, Nathan A ^a   Zhang, Yinhua ^a   Evans, Thomas C ^a   LaBarre, Paul ^b   Wanji, Samuel ^c   Burton, Robert A ^b   Carlow, Clotilde K S ^a  

^a NEW ENGLAND BIOLABS   (United States)

^b PATH   (United States)

^c Research Foundation in Tropical Diseases and Environment   (Cameroon)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; GENOMIC DNA; NEUTRAL RED; PHENOLSULFONPHTHALEIN; REPETITIVE DNA; HELMINTH DNA;

ARTICLE; BIOCHEMICAL EQUIPMENT; BRUGIA; COLORIMETRY; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DNA CONTENT; DNA DETERMINATION; FILARIASIS; GENE AMPLIFICATION; GENE DOSAGE; HUMAN; INFECTION CONTROL; INSECT CONTROL; NON INSTRUMENTED NUCLEIC ACID AMPLIFICATION DEVICE; NON INSTRUMENTED NUCLEIC ACID LOOP MEDIATED ISOTHERMAL AMPLIFICATION; NONHUMAN; NUCLEIC ACID ANALYSIS; ONCHOCERCA VOLVULUS; REACTION TIME; SENSITIVITY ANALYSIS; SPECIES DIFFERENCE; VECTOR SURVEILLANCE; WUCHERERIA BANCROFTI; AEDES; ANIMAL; ELEPHANTIASIS, FILARIAL; GENETICS; NUCLEIC ACID AMPLIFICATION; ONCHOCERCIASIS; PARASITOLOGY; PROCEDURES; SIMULIIDAE;

AEDES; ANIMALS; COLORIMETRY; DNA, HELMINTH; ELEPHANTIASIS, FILARIAL; HUMANS; NUCLEIC ACID AMPLIFICATION TECHNIQUES; ONCHOCERCA VOLVULUS; ONCHOCERCIASIS; SIMULIIDAE; WUCHERERIA BANCROFTI;

EID: 85013001161     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0169011     Document Type: Article

References (54)

1. Alhassan A, Li Z, Poole CB, Carlow CK. Expanding the MDx toolbox for filarial diagnosis and surveillance. Trends in parasitology. 2015.
2. WHO. Working to overcome the global impact of neglected tropical diseases: first WHO report on neglected tropical diseases WHO, 2010 WHO/HTM/NTD/2010.1.
3. WHO. Global programme to eliminate lymphatic filariasis progress report, 2011. Weekly Epidemiological Record. 2012;87:345-56. PMID: 22977952
4. Taylor MJ, Hoerauf A, Bockarie M. Lymphatic filariasis and onchocerciasis. Lancet. 2010;376(9747):1175-85. doi:10.1016/S0140-6736 (10) 60586-7 PMID: 20739055
5. Coffeng LE, Stolk WA, Zoure HG, Veerman JL, Agblewonu KB, Murdoch ME, et al. African Programme For Onchocerciasis Control 1995-2015: model-estimated health impact and cost. PLoS neglected tropical diseases. 2013;7(1):e2032. PubMed Central PMCID: PMC3561133. doi:10.1371/journal.pntd. 0002032 PMID: 23383355
6. Ton TG, Mackenzie C, Molyneux DH. The burden of mental health in lymphatic filariasis. Infectious diseases of poverty. 2015;4:34. PubMed Central PMCID: PMC4520254. doi:10.1186/s40249-015-0068-7 PMID: 26229599
7. Crump A, Morel CM, Omura S. The onchocerciasis chronicle: from the beginning to the end? Trends in parasitology. 2012;28(7):280-8. doi:10.1016/j.pt.2012.04.005 PMID: 22633470
8. Weil GJ, Ramzy RM. Diagnostic tools for filariasis elimination programs. Trends in parasitology. 2007;23(2):78-82. Epub 2006/12/19. doi:10.1016/j.pt.2006.12.001 PMID: 17174604
9. WHO. Global programme to eliminate lymphatic filariasis: monitoring and epidemiological assessment of mass drug administration. 2011 WHO/HTM/NTD/PCT/2011.4.
10. Steel C, Golden A, Kubofcik J, LaRue N, De Los Santos T, Domingo GJ, et al. Rapid Wuchereria bancroftispecific antigen Wb123-based IgG4 immunoassays as tools for surveillance following mass drug administration programs on lymphatic filariasis. Clinical and vaccine immunology: CVI. 2013;20(8):1155-61. PubMed Central PMCID: PMC3754496. doi:10.1128/CVI.00252-13 PMID: 23740923
11. Lammie PJ, Weil G, Noordin R, Kaliraj P, Steel C, Goodman D, et al. Recombinant antigen-based antibody assays for the diagnosis and surveillance of lymphatic filariasis-a multicenter trial. Filaria journal. 2004;3(1):9. Epub 2004/09/07. PubMed Central PMCID: PMC519021. doi:10.1186/1475-2883-3-9 PMID: 15347425
12. Fischer P, Bonow I, Supali T, Ruckert P, Rahmah N. Detection of filaria-specific IgG4 antibodies and filarial DNA, for the screening of blood spots for Brugia timori. Annals of tropical medicine and parasitology. 2005;99(1):53-60. Epub 2005/02/11. doi:10.1179/136485905X13339 PMID: 15701256
13. Joseph H, Maiava F, Naseri T, Taleo F, Ake M, Capuano C, et al. Application of the Filariasis CELISA Antifilarial IgG (4) Antibody Assay in Surveillance in Lymphatic Filariasis Elimination Programmes in the South Pacific. Journal of tropical medicine. 2011;2011:492023. PubMed Central PMCID: PMC3180782. doi:10.1155/2011/492023 PMID: 21961018
14. Lobos E, Weiss N, Karam M, Taylor HR, Ottesen EA, Nutman TB. An immunogenic Onchocerca volvulus antigen: a specific and early marker of infection. Science. 1991;251(5001):1603-5. PMID: 2011741
15. Oguttu D, Byamukama E, Katholi CR, Habomugisha P, Nahabwe C, Ngabirano M, et al. Serosurveillance to monitor onchocerciasis elimination: the Ugandan experience. The American journal of tropical medicine and hygiene. 2014;90(2):339-45. PubMed Central PMCID: PMC3919245. doi:10.4269/ajtmh.13-0546 PMID: 24343885
16. Gounoue-Kamkumo R, Nana-Djeunga HC, Bopda J, Akame J, Tarini A, Kamgno J. Loss of sensitivity of immunochromatographic test (ICT) for lymphatic filariasis diagnosis in low prevalence settings: consequence in the monitoring and evaluation procedures. BMC infectious diseases. 2015;15:579. PubMed Central PMCID: PMC4690254. doi:10.1186/s12879-015-1317-x PMID: 26700472
17. Luz SL, Crainey JL, Shelley AJ, Rubio M. Outstanding insecurities concerning the use of an Ov16-based ELISA in the Amazonia onchocerciasis focus. Memorias do Instituto Oswaldo Cruz. 2014;109(4):506-8. PubMed Central PMCID: PMC4155858. doi:10.1590/0074-0276140079 PMID: 25075790
18. Bakajika DK, Nigo MM, Lotsima JP, Masikini GA, Fischer K, Lloyd MM, et al. Filarial antigenemia and Loa loa night blood microfilaremia in an area without bancroftian filariasis in the Democratic Republic of Congo. The American journal of tropical medicine and hygiene. 2014;91(6):1142-8. PubMed Central PMCID: PMC4257636. doi:10.4269/ajtmh.14-0358 PMID: 25223938
19. Okorie PN, De Souza DK. Prospects, drawbacks and future needs of xenomonitoring for the endpoint evaluation of lymphatic filariasis elimination programs in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2016;110(2):90-7. doi:10.1093/trstmh/trv104 PMID: 26822601
20. Osei-Atweneboana MY, Boakye DA, Awadzi K, Gyapong JO, Prichard RK. Genotypic analysis of betatubulin in Onchocerca volvulus from communities and individuals showing poor parasitological response to ivermectin treatment. International journal for parasitology Drugs and drug resistance. 2012;2:20-8. PubMed Central PMCID: PMC3862422. doi:10.1016/j.ijpddr.2012.01.005 PMID: 24533268
21. Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, et al. Loop-mediated isothermal amplification of DNA. Nucleic acids research. 2000;28(12):E63. Epub 2000/06/28. PubMed Central PMCID: PMC102748. PMID: 10871386
22. Notomi T, Mori Y, Tomita N, Kanda H. Loop-mediated isothermal amplification (LAMP): principle, features, and future prospects. J Microbiol. 2015;53(1):1-5. doi:10.1007/s12275-015-4656-9 PMID: 25557475
23. Kaneko H, Kawana T, Fukushima E, Suzutani T. Tolerance of loop-mediated isothermal amplification to a culture medium and biological substances. Journal of biochemical and biophysical methods. 2007;70(3):499-501. doi:10.1016/j.jbbm.2006.08.008 PMID: 17011631
24. Poon LL, Wong BW, Ma EH, Chan KH, Chow LM, Abeyewickreme W, et al. Sensitive and inexpensive molecular test for falciparum malaria: detecting Plasmodium falciparum DNA directly from heat-treated blood by loop-mediated isothermal amplification. Clinical chemistry. 2006;52(2):303-6. doi:10.1373/clinchem.2005.057901 PMID: 16339303
25. Alhassan A, Makepeace BL, LaCourse EJ, Osei-Atweneboana MY, Carlow CK. A simple isothermal DNA amplification method to screen black flies for Onchocerca volvulus infection. PloS one. 2014;9(10):e108927. PubMed Central PMCID: PMC4191976. doi:10.1371/journal.pone.0108927 PMID: 25299656
26. Mori Y, Hirano T, Notomi T. Sequence specific visual detection of LAMP reactions by addition of cationic polymers. BMC biotechnology. 2006;6:3. Epub 2006/01/13. PubMed Central PMCID: PMC1373654. doi:10.1186/1472-6750-6-3 PMID: 16401354
27. Tomita N, Mori Y, Kanda H, Notomi T. Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products. Nature protocols. 2008;3(5):877-82. Epub 2008/05/03. doi:10.1038/nprot.2008.57 PMID: 18451795
28. Goto M, Honda E, Ogura A, Nomoto A, Hanaki K. Colorimetric detection of loop-mediated isothermal amplification reaction by using hydroxy naphthol blue. Biotechniques. 2009;46(3):167-72. Epub 2009/03/26. doi:10.2144/000113072 PMID: 19317660
29. Lucchi NW, Demas A, Narayanan J, Sumari D, Kabanywanyi A, Kachur SP, et al. Real-time fluorescence loop mediated isothermal amplification for the diagnosis of malaria. PloS one. 2010;5(10):e13733. Epub 2010/11/10. PubMed Central PMCID: PMC2966401. doi:10.1371/journal.pone.0013733 PMID: 21060829
30. Poole CB, Tanner NA, Zhang Y, Evans TC Jr., Carlow CK. Diagnosis of brugian filariasis by loop-mediated isothermal amplification. PLoS neglected tropical diseases. 2012;6(12):e1948. PubMed Central PMCID: PMC3521703. doi:10.1371/journal.pntd.0001948 PMID: 23272258
31. Fernandez-Soto P, Mvoulouga PO, Akue JP, Aban JL, Santiago BV, Sanchez MC, et al. Development of a highly sensitive loop-mediated isothermal amplification (LAMP) method for the detection of Loa loa. PloS one. 2014;9(4):e94664. PubMed Central PMCID: PMC3983228. doi:10.1371/journal.pone. 0094664 PMID: 24722638
32. Poole CB, Ettwiller L, Tanner NA, Evans TC, Jr., Wanji S, Carlow CK. Genome Filtering for New DNA Biomarkers of Loa loa Infection Suitable for Loop-Mediated Isothermal Amplification. PloS one. 2015;10(9):e0139286. PubMed Central PMCID: PMC4586141. doi:10.1371/journal.pone.0139286 PMID: 26414073
33. Takagi H, Itoh M, Kasai S, Yahathugoda TC, Weerasooriya MV, Kimura E. Development of loop-mediated isothermal amplification method for detecting Wuchereria bancrofti DNA in human blood and vector mosquitoes. Parasitology international. 2011;60(4):493-7. Epub 2011/09/21. doi:10.1016/j.parint. 2011.08.018 PMID: 21930238
34. Curtis KA, Rudolph DL, Nejad I, Singleton J, Beddoe A, Weigl B, et al. Isothermal amplification using a chemical heating device for point-of-care detection of HIV-1. PloS one. 2012;7(2):e31432. PubMed Central PMCID: PMC3285652. doi:10.1371/journal.pone.0031432 PMID: 22384022
35. Singleton J, Osborn JL, Lillis L, Hawkins K, Guelig D, Price W, et al. Electricity-free amplification and detection for molecular point-of-care diagnosis of HIV-1. PloS one. 2014;9(11):e113693. PubMed Central PMCID: PMC4245218. doi:10.1371/journal.pone.0113693 PMID: 25426953
36. Sema M, Alemu A, Bayih AG, Getie S, Getnet G, Guelig D, et al. Evaluation of non-instrumented nucleic acid amplification by loop-mediated isothermal amplification (NINA-LAMP) for the diagnosis of malaria in Northwest Ethiopia. Malaria journal. 2015;14:44. PubMed Central PMCID: PMC4323137. doi:10.1186/s12936-015-0559-9 PMID: 25626339
37. Buser JR, Diesburg S, Singleton J, Guelig D, Bishop JD, Zentner C, et al. Precision chemical heating for diagnostic devices. Lab on a chip. 2015;15(23):4423-32. doi:10.1039/c5lc01053e PMID: 26503640
38. Tanner NA, Zhang Y, Evans TC Jr. Visual detection of isothermal nucleic acid amplification using pHsensitive dyes. Biotechniques. 2015;58(2):59-68. doi:10.2144/000114253 PMID: 25652028
39. Wanji S, Kengne-Ouafo JA, Esum ME, Chounna PW, Tendongfor N, Adzemye BF, et al. Situation analysis of parasitological and entomological indices of onchocerciasis transmission in three drainage basins of the rain forest of South West Cameroon after a decade of ivermectin treatment. Parasites & vectors. 2015;8:202. PubMed Central PMCID: PMC4393872.
40. Nagamine K, Hase T, Notomi T. Accelerated reaction by loop-mediated isothermal amplification using loop primers. Molecular and cellular probes. 2002;16(3):223-9. Epub 2002/07/30. PMID: 12144774
41. Poole CB, Williams SA. A rapid DNA assay for the species-specific detection and quantification of Brugia in blood samples. Molecular and biochemical parasitology. 1990;40(1):129-36. Epub 1990/04/01. PMID: 2348829
42. Sergev SS, Black SA, Jenkins JF, inventors Supercorroding galvanic cell alloys for generation of heat and gas patent US 4264362 A. 1981.
43. Lizotte MR, Supali T, Partono F, Williams SA. A polymerase chain reaction assay for the detection of Brugia malayi in blood. American journal of tropical medicine and hygiene. 1994;51(3):314-21. Epub 1994/09/01. PMID: 7943550
44. Noordin R, Aziz RA, Ravindran B. Homologs of the Brugia malayi diagnostic antigen BmR1 are present in other filarial parasites but induce different humoral immune responses. Filaria journal. 2004;3(1):10. PubMed Central PMCID: PMC544840. doi:10.1186/1475-2883-3-10 PMID: 15627400
45. Kouassi BL, De Souza DK, Goepogui A, Narh CA, King SA, Mamadou BS, et al. Assessing the presence of Wuchereria bancrofti in vector and human populations from urban communities in Conakry, Guinea. Parasites & vectors. 2015;8:492. PubMed Central PMCID: PMC4583765.
46. Wahl G, Ekale D, Schmitz A. Onchocerca ochengi: assessment of the Simulium vectors in north Cameroon. Parasitology. 1998;116(Pt 4):327-36.
47. Meredith SE, Unnasch TR, Karam M, Piessens WF, Wirth DF. Cloning and characterization of an Onchocerca volvulus specific DNA sequence. Molecular and biochemical parasitology. 1989;36(1):1-10. PMID: 2811941
48. Meredith SE, Lando G, Gbakima AA, Zimmerman PA, Unnasch TR. Onchocerca volvulus: application of the polymerase chain reaction to identification and strain differentiation of the parasite. Experimental parasitology. 1991;73(3):335-44. PMID: 1915748
49. Merriweather A, Unnasch TR. Onchocerca volvulus: development of a species specific polymerase chain reaction-based assay. Experimental parasitology. 1996;83(1):164-6. doi:10.1006/expr.1996. 0062 PMID: 8654547
50. Rao RU, Atkinson LJ, Ramzy RM, Helmy H, Farid HA, Bockarie MJ, et al. A real-time PCR-based assay for detection of Wuchereria bancrofti DNA in blood and mosquitoes. The American journal of tropical medicine and hygiene. 2006;74(5):826-32. Epub 2006/05/12. PubMed Central PMCID: PMC2196401. PMID: 16687688
51. Drame PM, Fink DL, Kamgno J, Herrick JA, Nutman TB. Loop-mediated isothermal amplification for rapid and semiquantitative detection of Loa loa infection. J Clin Microbiol. 2014;52(6):2071-7. PubMed Central PMCID: PMC4042750. doi:10.1128/JCM.00525-14 PMID: 24696020
52. McCarthy JS, Lustigman S, Yang GJ, Barakat RM, Garcia HH, Sripa B, et al. A research agenda for helminth diseases of humans: diagnostics for control and elimination programmes. PLoS neglected tropical diseases. 2012;6(4):e1601. Epub 2012/05/01. PubMed Central PMCID: PMC3335877. doi:10. 1371/journal.pntd.0001601 PMID: 22545166
53. Wanji S, Amvongo-Adjia N, Koudou B, Njouendou AJ, Chounna Ndongmo PW, Kengne-Ouafo JA, et al. Cross-Reactivity of Filariais ICT Cards in Areas of Contrasting Endemicity of Loa loa and Mansonella perstans in Cameroon: Implications for Shrinking of the Lymphatic Filariasis Map in the Central African Region. PLoS neglected tropical diseases. 2015;9(11):e0004184. PubMed Central PMCID: PMC4636288. doi:10.1371/journal.pntd.0004184 PMID: 26544042
54. Wanji S, Amvongo-Adjia N, Njouendou AJ, Kengne-Ouafo JA, Ndongmo WP, Fombad FF, et al. Further evidence of the cross-reactivity of the Binax NOW (R) Filariasis ICT cards to non-Wuchereria bancrofti filariae: experimental studies with Loa loa and Onchocerca ochengi. Parasites & vectors. 2016;9(1):267. PubMed Central PMCID: PMC4858834.