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Diagnosis of Brugian Filariasis by Loop-Mediated Isothermal Amplification

DOI: 10.1371/journal.pntd.0001948

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Abstract:

In this study we developed and evaluated a Brugia Hha I repeat loop-mediated isothermal amplification (LAMP) assay for the rapid detection of Brugia genomic DNA. Amplification was detected using turbidity or fluorescence as readouts. Reactions generated a turbidity threshold value or a clear visual positive within 30 minutes using purified genomic DNA equivalent to one microfilaria. Similar results were obtained using DNA isolated from blood samples containing B. malayi microfilariae. Amplification was specific to B. malayi and B. timori, as no turbidity was observed using DNA from the related filarial parasites Wuchereria bancrofti, Onchocerca volvulus or Dirofilaria immitis, or from human or mosquito. Furthermore, the assay was most robust using a new strand-displacing DNA polymerase termed Bst 2.0 compared to wild-type Bst DNA polymerase, large fragment. The results indicate that the Brugia Hha I repeat LAMP assay is rapid, sensitive and Brugia-specific with the potential to be developed further as a field tool for diagnosis and mapping of brugian filariasis.

References

[1]  WHO (2004) Regional Strategic Plan for Elimination of Lymphatic Filariasis (2004–2007). New Delhi: World Health Organization Regional Office for South-East Asia. SEA-FIL-29 SEA-FIL-29.
[2]  Ottesen EA (2006) Lymphatic filariasis: Treatment, control and elimination. Adv Parasitol 61: 395–441. doi: 10.1016/S0065-308X(05)61010-X
[3]  WHO (2008) Global programme to eliminate lymphatic filariasis. Wkly Epidemiol Rec 83: 333–341.
[4]  Weil GJ, Lammie PJ, Weiss N (1997) The ICT Filariasis Test: A rapid-format antigen test for diagnosis of bancroftian filariasis. Parasitol Today 13: 401–404. doi: 10.1016/S0169-4758(97)01130-7
[5]  McCarthy JS, Lustigman S, Yang GJ, Barakat RM, Garcia HH, et al. (2012) A research agenda for helminth diseases of humans: diagnostics for control and elimination programmes. PLoS Negl Trop Dis 6: e1601. doi: 10.1371/journal.pntd.0001601
[6]  WHO (2005) Sixth meeting of the Technical Advisory Group on the Global Elimination of Lymphatic Filariasis, Geneva, Switzerland, 20–23 September 2005. Wkly Epidemiol Rec 80: 401–408.
[7]  Weil GJ, Ramzy RM (2007) Diagnostic tools for filariasis elimination programs. Trends Parasitol 23: 78–82. doi: 10.1016/j.pt.2006.12.001
[8]  Rao KV, Eswaran M, Ravi V, Gnanasekhar B, Narayanan RB, et al. (2000) The Wuchereria bancrofti orthologue of Brugia malayi SXP1 and the diagnosis of bancroftian filariasis. Mol Biochem Parasitol 107: 71–80. doi: 10.1016/S0166-6851(99)00231-5
[9]  Vincent JA, Lustigman S, Zhang S, Weil GJ (2000) A comparison of newer tests for the diagnosis of onchocerciasis. Ann Trop Med Parasitol 94: 253–258. doi: 10.1080/00034980050006438
[10]  Lammie PJ, Weil G, Noordin R, Kaliraj P, Steel C, et al. (2004) Recombinant antigen-based antibody assays for the diagnosis and surveillance of lymphatic filariasis - a multicenter trial. Filaria J 3: 9. doi: 10.1186/1475-2883-3-9
[11]  Lizotte MR, Supali T, Partono F, Williams SA (1994) A polymerase chain reaction assay for the detection of Brugia malayi in blood. Am J Trop Med Hyg 51: 314–321.
[12]  Rahmah N, Ashikin AN, Anuar AK, Ariff RH, Abdullah B, et al. (1998) PCR-ELISA for the detection of Brugia malayi infection using finger-prick blood. Trans R Soc Trop Med Hyg 92: 404–406. doi: 10.1016/S0035-9203(98)91066-5
[13]  Kluber S, Supali T, Williams SA, Liebau E, Fischer P (2001) Rapid PCR-based detection of Brugia malayi DNA from blood spots by DNA Detection Test Strips. Trans R Soc Trop Med Hyg 95: 169–170. doi: 10.1016/S0035-9203(01)90148-8
[14]  Rao RU, Weil GJ, Fischer K, Supali T, Fischer P (2006) Detection of Brugia parasite DNA in human blood by real-time PCR. J Clin Microbiol 44: 3887–3893. doi: 10.1128/JCM.00969-06
[15]  Fischer P, Wibowo H, Pischke S, Ruckert P, Liebau E, et al. (2002) PCR-based detection and identification of the filarial parasite Brugia timori from Alor Island, Indonesia. Ann Trop Med Parasitol 96: 809–821. doi: 10.1179/000349802125002239
[16]  Fischer P, Bonow I, Supali T, Ruckert P, Rahmah N (2005) Detection of filaria-specific IgG4 antibodies and filarial DNA, for the screening of blood spots for Brugia timori. Ann Trop Med Parasitol 99: 53–60. doi: 10.1179/136485905X13339
[17]  Chansiri K, Phantana S (2002) A polymerase chain reaction assay for the survey of bancroftian filariasis. Southeast Asian J Trop Med Public Health 33: 504–508.
[18]  Fink DL, Fahle GA, Fischer S, Fedorko DF, Nutman TB (2011) Toward molecular parasitologic diagnosis: enhanced diagnostic sensitivity for filarial infections in mobile populations. J Clin Microbiol 49: 42–47. doi: 10.1128/JCM.01697-10
[19]  Hassan M, Sanad MM, el-Karamany I, Abdel-Tawab M, Shalaby M, et al. (2005) Detection of DNA of W. bancrofti in blood samples by QC-PCR-ELISA-based. J Egypt Soc Parasitol 35: 963–970.
[20]  Ramzy RM, Farid HA, Kamal IH, Ibrahim GH, Morsy ZS, et al. (1997) A polymerase chain reaction-based assay for detection of Wuchereria bancrofti in human blood and Culex pipiens. Trans R Soc Trop Med Hyg 91: 156–160. doi: 10.1016/S0035-9203(97)90205-4
[21]  Rao RU, Atkinson LJ, Ramzy RM, Helmy H, Farid HA, et al. (2006) A real-time PCR-based assay for detection of Wuchereria bancrofti DNA in blood and mosquitoes. Am J Trop Med Hyg 74: 826–832.
[22]  Zhong M, McCarthy J, Bierwert L, Lizotte-Waniewski M, Chanteau S, et al. (1996) A polymerase chain reaction assay for detection of the parasite Wuchereria bancrofti in human blood samples. Am J Trop Med Hyg 54: 357–363.
[23]  Bockarie MJ, Fischer P, Williams SA, Zimmerman PA, Griffin L, et al. (2000) Application of a polymerase chain reaction-ELISA to detect Wuchereria bancrofti in pools of wild-caught Anopheles punctulatus in a filariasis control area in Papua New Guinea. Am J Trop Med Hyg 62: 363–367.
[24]  Fischer P, Liu X, Lizotte-Waniewski M, Kamal IH, Ramzy RM, et al. (1999) Development of a quantitative, competitive polymerase chain reaction–enzyme-linked immunosorbent assay for the detection of Wuchereria bancrofti DNA. Parasitol Res 85: 176–183. doi: 10.1007/s004360050531
[25]  Goodman DS, Orelus JN, Roberts JM, Lammie PJ, Streit TG (2003) PCR and Mosquito dissection as tools to monitor filarial infection levels following mass treatment. Filaria J 2: 11. doi: 10.1186/1475-2883-2-11
[26]  Helmy H, Fischer P, Farid HA, Bradley MH, Ramzy RM (2004) Test strip detection of Wuchereria bancrofti amplified DNA in wild-caught Culex pipiens and estimation of infection rate by a PoolScreen algorithm. Trop Med Int Health 9: 158–163. doi: 10.1046/j.1365-3156.2003.01155.x
[27]  Intapan PM, Thanchomnang T, Lulitanond V, Maleewong W (2009) Rapid detection of Wuchereria bancrofti and Brugia malayi in mosquito vectors (Diptera: Culicidae) using a real-time fluorescence resonance energy transfer multiplex PCR and melting curve analysis. J Med Entomol 46: 158–164. doi: 10.1603/033.046.0119
[28]  Ramzy RM, El Setouhy M, Helmy H, Ahmed ES, Abd Elaziz KM, et al. (2006) Effect of yearly mass drug administration with diethylcarbamazine and albendazole on bancroftian filariasis in Egypt: a comprehensive assessment. Lancet 367: 992–999. doi: 10.1016/S0140-6736(06)68426-2
[29]  Williams SA, Laney SJ, Bierwert LA, Saunders LJ, Boakye DA, et al. (2002) Development and standardization of a rapid, PCR-based method for the detection of Wuchereria bancrofti in mosquitoes, for xenomonitoring the human prevalence of bancroftian filariasis. Ann Trop Med Parasitol 96 Suppl 2: S41–46. doi: 10.1179/000349802125002356
[30]  Laney SJ, Buttaro CJ, Visconti S, Pilotte N, Ramzy RM, et al. (2008) A reverse transcriptase-PCR assay for detecting filarial infective larvae in mosquitoes. PLoS Negl Trop Dis 2: e251. doi: 10.1371/journal.pntd.0000251
[31]  Thanchomnang T, Intapan PM, Lulitanond V, Choochote W, Manjai A, et al. (2008) Rapid detection of Brugia malayi in mosquito vectors using a real-time fluorescence resonance energy transfer PCR and melting curve analysis. Am J Trop Med Hyg 78: 509–513.
[32]  Vasuki V, Patra KP, Hoti SL (2001) A rapid and simplified method of DNA extraction for the detection of Brugia malayi infection in mosquitoes by PCR assay. Acta Trop 79: 245–248. doi: 10.1016/S0001-706X(01)00136-X
[33]  Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, et al. (2000) Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 28: E63. doi: 10.1093/nar/28.12.e63
[34]  Nagamine K, Hase T, Notomi T (2002) Accelerated reaction by loop-mediated isothermal amplification using loop primers. Mol Cell Probes 16: 223–229. doi: 10.1006/mcpr.2002.0415
[35]  Nagamine K, Watanabe K, Ohtsuka K, Hase T, Notomi T (2001) Loop-mediated isothermal amplification reaction using a nondenatured template. Clin Chem 47: 1742–1743.
[36]  Han ET, Watanabe R, Sattabongkot J, Khuntirat B, Sirichaisinthop J, et al. (2007) Detection of four Plasmodium species by genus- and species-specific loop-mediated isothermal amplification for clinical diagnosis. J Clin Microbiol 45: 2521–2528. doi: 10.1128/JCM.02117-06
[37]  Iseki H, Alhassan A, Ohta N, Thekisoe OM, Yokoyama N, et al. (2007) Development of a multiplex loop-mediated isothermal amplification (mLAMP) method for the simultaneous detection of bovine Babesia parasites. J Microbiol Methods 71: 281–287. doi: 10.1016/j.mimet.2007.09.019
[38]  Aonuma H, Suzuki M, Iseki H, Perera N, Nelson B, et al. (2008) Rapid identification of Plasmodium-carrying mosquitoes using loop-mediated isothermal amplification. Biochem Biophys Res Commun 376: 671–676. doi: 10.1016/j.bbrc.2008.09.061
[39]  Kuboki N, Inoue N, Sakurai T, Di Cello F, Grab DJ, et al. (2003) Loop-mediated isothermal amplification for detection of African trypanosomes. J Clin Microbiol 41: 5517–5524. doi: 10.1128/JCM.41.12.5517-5524.2003
[40]  Njiru ZK, Mikosza AS, Armstrong T, Enyaru JC, Ndung'u JM, et al. (2008) Loop-mediated isothermal amplification (LAMP) method for rapid detection of Trypanosoma brucei rhodesiense. PLoS Negl Trop Dis 2: e147. doi: 10.1371/journal.pntd.0000147
[41]  Nkouawa A, Sako Y, Li T, Chen X, Wandra T, et al. (2010) Evaluation of a loop-mediated isothermal amplification method using fecal specimens for differential detection of Taenia species from humans. J Clin Microbiol 48: 3350–3352. doi: 10.1128/JCM.00697-10
[42]  Paris DH, Imwong M, Faiz AM, Hasan M, Yunus EB, et al. (2007) Loop-mediated isothermal PCR (LAMP) for the diagnosis of falciparum malaria. Am J Trop Med Hyg 77: 972–976.
[43]  Takagi H, Itoh M, Kasai S, Yahathugoda TC, Weerasooriya MV, et al. (2011) Development of loop-mediated isothermal amplification method for detecting Wuchereria bancrofti DNA in human blood and vector mosquitoes. Parasitol Int 60: 493–497. doi: 10.1016/j.parint.2011.08.018
[44]  Thekisoe OM, Rodriguez CV, Rivas F, Coronel-Servian AM, Fukumoto S, et al. (2010) Detection of Trypanosoma cruzi and T. rangeli infections from Rhodnius pallescens bugs by loop-mediated isothermal amplification (LAMP). Am J Trop Med Hyg 82: 855–860. doi: 10.4269/ajtmh.2010.09-0533
[45]  Abbasi I, King CH, Muchiri EM, Hamburger J (2010) Detection of Schistosoma mansoni and Schistosoma haematobium DNA by loop-mediated isothermal amplification: identification of infected snails from early prepatency. Am J Trop Med Hyg 83: 427–432. doi: 10.4269/ajtmh.2010.09-0764
[46]  Geojith G, Dhanasekaran S, Chandran SP, Kenneth J (2011) Efficacy of loop mediated isothermal amplification (LAMP) assay for the laboratory identification of Mycobacterium tuberculosis isolates in a resource limited setting. J Microbiol Methods 84: 71–73. doi: 10.1016/j.mimet.2010.10.015
[47]  Endo S, Komori T, Ricci G, Sano A, Yokoyama K, et al. (2004) Detection of gp43 of Paracoccidioides brasiliensis by the loop-mediated isothermal amplification (LAMP) method. FEMS Microbiol Lett 234: 93–97. doi: 10.1016/j.femsle.2004.03.015
[48]  Ihira M, Yoshikawa T, Enomoto Y, Akimoto S, Ohashi M, et al. (2004) Rapid diagnosis of human herpesvirus 6 infection by a novel DNA amplification method, loop-mediated isothermal amplification. J Clin Microbiol 42: 140–145. doi: 10.1128/JCM.42.1.140-145.2004
[49]  Pham HM, Nakajima C, Ohashi K, Onuma M (2005) Loop-mediated isothermal amplification for rapid detection of Newcastle disease virus. J Clin Microbiol 43: 1646–1650. doi: 10.1128/JCM.43.4.1646-1650.2005
[50]  Boehme CC, Nabeta P, Henostroza G, Raqib R, Rahim Z, et al. (2007) Operational feasibility of using loop-mediated isothermal amplification for diagnosis of pulmonary tuberculosis in microscopy centers of developing countries. J Clin Microbiol 45: 1936–1940. doi: 10.1128/JCM.02352-06
[51]  Mitarai S, Okumura M, Toyota E, Yoshiyama T, Aono A, et al. (2011) Evaluation of a simple loop-mediated isothermal amplification test kit for the diagnosis of tuberculosis. Int J Tuberc Lung Dis 15: 1211–1217, i. doi: 10.5588/ijtld.10.0629
[52]  Matovu E, Kazibwe AJ, Mugasa CM, Ndungu JM, Njiru ZK (2012) Towards Point-of-Care Diagnostic and Staging Tools for Human African Trypanosomiaisis. J Trop Med 2012: 340538. doi: 10.1155/2012/340538
[53]  Chularerk P, Desowitz RS (1970) A simplified membrane filtration technique for the diagnosis of microfilaremia. J Parasitol 56: 623–624. doi: 10.2307/3277640
[54]  Dennis DT, Kean BH (1971) Isolation of microfilariae: report of a new method. J Parasitol 57: 1146–1147. doi: 10.2307/3277886
[55]  Lim PKC, Sim BKL (1983) Laboratory Techniques in Filariasis. In: Mak JW, editor. Bulletin No 19. Malaysia: Institute for Medical Research. pp. 95–104.
[56]  Muller R, Wakelin D (2002) Helminthological Techniques. Worms and Human Disease. 2 ed. NewYork: CABI Publishing. pp. 256–270.
[57]  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. doi: 10.1093/nar/22.22.4673
[58]  McReynolds LA, DeSimone SM, Williams SA (1986) Cloning and comparison of repeated DNA sequences from the human filarial parasite Brugia malayi and the animal parasite Brugia pahangi. Proc Natl Acad Sci U S A 83: 797–801. doi: 10.1073/pnas.83.3.797
[59]  Casinader Saverimuttu JK, Karunanayake EH, Chandrasekharan NV, Jayasena SM (2000) Molecular characterisation of the actin gene of the filarial parasite Wuchereria bancrofti. Int J Parasitol 30: 119–124. doi: 10.1016/S0020-7519(99)00176-9
[60]  Zeng W, Donelson JE (1992) The actin genes of Onchocerca volvulus. Mol Biochem Parasitol 55: 207–216. doi: 10.1016/0166-6851(92)90141-6
[61]  Tomita N, Mori Y, Kanda H, Notomi T (2008) Loop-mediated isothermal amplification (LAMP) of gene sequences and simple visual detection of products. Nat Protoc 3: 877–882. doi: 10.1038/nprot.2008.57
[62]  Ghedin E, Wang S, Spiro D, Caler E, Zhao Q, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 317: 1756–1760. doi: 10.1126/science.1145406
[63]  Fischer P, Supali T, Wibowo H, Bonow I, Williams SA (2000) Detection of DNA of nocturnally periodic Brugia malayi in night and day blood samples by a polymerase chain reaction-ELISA-based method using an internal control DNA. Am J Trop Med Hyg 62: 291–296.
[64]  Melrose WD (2002) Lymphatic filariasis: new insights into an old disease. Int J Parasitol 32: 947–960. doi: 10.1016/S0020-7519(02)00062-0
[65]  Tanner NA, Zhang Y, Evans TC Jr (2012) Simultaneous multiple target detection in real-time loop-mediated isothermal amplification. Biotechniques 53: 81–89. doi: 10.2144/0000113902
[66]  Kellogg DE, Rybalkin I, Chen S, Mukhamedova N, Vlasik T, et al. (1994) TaqStart Antibody: “hot start” PCR facilitated by a neutralizing monoclonal antibody directed against Taq DNA polymerase. Biotechniques 16: 1134–1137.
[67]  Kimura Y, de Hoon MJ, Aoki S, Ishizu Y, Kawai Y, et al. (2011) Optimization of turn-back primers in isothermal amplification. Nucleic Acids Res 39: e59. doi: 10.1093/nar/gkr041
[68]  Xie H, Bain O, Williams SA (1994) Molecular phylogenetic studies on Brugia filariae using Hha I repeat sequences. Parasite 1: 255–260.
[69]  Aonuma H, Yoshimura A, Kobayashi T, Okado K, Badolo A, et al. (2010) A single fluorescence-based LAMP reaction for identifying multiple parasites in mosquitoes. Exp Parasitol 125: 179–183. doi: 10.1016/j.exppara.2009.12.023
[70]  Aonuma H, Yoshimura A, Perera N, Shinzawa N, Bando H, et al. (2009) Loop-mediated isothermal amplification applied to filarial parasites detection in the mosquito vectors: Dirofilaria immitis as a study model. Parasit Vectors 2: 15. doi: 10.1186/1756-3305-2-15
[71]  Cho HS, Park NY (2005) Detection of canine distemper virus in blood samples by reverse transcription loop-mediated isothermal amplification. J Vet Med B Infect Dis Vet Public Health 52: 410–413. doi: 10.1111/j.1439-0450.2005.00886.x
[72]  Mori Y, Hirano T, Notomi T (2006) Sequence specific visual detection of LAMP reactions by addition of cationic polymers. BMC Biotechnol 6: 3. doi: 10.1186/1472-6750-6-3
[73]  Savan R, Kono T, Itami T, Sakai M (2005) Loop-mediated isothermal amplification: an emerging technology for detection of fish and shellfish pathogens. J Fish Dis 28: 573–581. doi: 10.1111/j.1365-2761.2005.00670.x
[74]  Curtis KA, Rudolph DL, Owen SM (2008) Rapid detection of HIV-1 by reverse-transcription, loop-mediated isothermal amplification (RT-LAMP). J Virol Methods 151: 264–270. doi: 10.1016/j.jviromet.2008.04.011
[75]  Dukes JP, King DP, Alexandersen S (2006) Novel reverse transcription loop-mediated isothermal amplification for rapid detection of foot-and-mouth disease virus. Arch Virol 151: 1093–1106. doi: 10.1007/s00705-005-0708-5
[76]  Iwamoto T, Sonobe T, Hayashi K (2003) Loop-mediated isothermal amplification for direct detection of Mycobacterium tuberculosis complex, M. avium, and M. intracellulare in sputum samples. J Clin Microbiol 41: 2616–2622. doi: 10.1128/JCM.41.6.2616-2622.2003
[77]  Lucchi NW, Demas A, Narayanan J, Sumari D, Kabanywanyi A, et al. (2010) Real-time fluorescence loop mediated isothermal amplification for the diagnosis of malaria. PLoS One 5: e13733. doi: 10.1371/journal.pone.0013733
[78]  Maruyama F, Kenzaka T, Yamaguchi N, Tani K, Nasu M (2003) Detection of bacteria carrying the stx2 gene by in situ loop-mediated isothermal amplification. Appl Environ Microbiol 69: 5023–5028. doi: 10.1128/AEM.69.8.5023-5028.2003
[79]  Qiao YM, Guo YC, Zhang XE, Zhou YF, Zhang ZP, et al. (2007) Loop-mediated isothermal amplification for rapid detection of Bacillus anthracis spores. Biotechnol Lett 29: 1939–1946. doi: 10.1007/s10529-007-9472-9
[80]  Goto M, Honda E, Ogura A, Nomoto A, Hanaki K (2009) Colorimetric detection of loop-mediated isothermal amplification reaction by using hydroxy naphthol blue. Biotechniques 46: 167–172. doi: 10.2144/000113072
[81]  Li S, Fang M, Zhou B, Ni H, Shen Q, et al. (2011) Simultaneous detection and differentiation of dengue virus serotypes 1–4, Japanese encephalitis virus, and West Nile virus by a combined reverse-transcription loop-mediated isothermal amplification assay. Virol J 8: 360. doi: 10.1186/1743-422X-8-360

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