Lymphatic filariasis (LF) remains a public health concern as it can cause permanent morbidity and disability to those infected. While the global elimination of LF in these endemic areas is ongoing through mass drug administration, there is the need to develop diagnostic tools that would be utilized to track the progress of total global eradication as well as perform surveillance for the recurrence of lymphatic filariasis transmission. Currently, approved LF diagnosis tools are faced with lack of specificity, low sensitivity, and periodicity dependence. Recombinant filarial antigen-based assays can address these drawbacks and offer practical instruments for LF diagnosis and surveillance. This present study, evaluated rWb-SXP-1 and rWb-123 antigens as potential diagnostic biomarker tools for Wuchereria banchrofti in human sera using microspheres-based multiplex serological assay. Based on statistical analysis using XLSTAT 2019 (Addinsoft) on data generated from multiplex technology assay, generated ROC curves for both rWb-SXP-1 and rWb-123 demonstrated 87.1% sensitivity to Wuchereria banchrofti human sera with rWb-SXP-1 antigens having the highest specificity of 96%. Indication that rWb-SXP-1 and rWb-123 antigens are capable of detecting immunoglobulin G4 (IgG4) antibodies in human sera synthesized specifically against W. banchrofti infections. Therefore, rWb-SXP-1 and rWb-123 antigens can be utilized to detect W. banchrofti infections by antibody profiling with excellent diagnostic sensitivity and specificity using microsphere-based multiplex serological tests. This method can be particularly practical for screening a large number of sera samples and/or for quick, extensive field-testing due to the high-throughput and quick formats applied.
References
[1]
Allen, S.P., Polazzi, J.O., Gierse, J.K. and Easton, A.M. (1992) Two Novel Heat Shock Genes Encoding Proteins Produced in Response to Heterologous Protein Expression in Escherichia coli. Journal of Bacteriology, 174, 6938-6947.
https://doi.org/10.1128/jb.174.21.6938-6947.1992
[2]
Baskar, L.K.V., Srikanth, T.R., Suba, S., Mody, H.C., Desai, P.K. and Kaliraj, P. (2004) Development and Evaluation of a Rapid Flow-Through Immunofiltration Test Using Recombinant Filarial Antigen for Diagnosis of Brugian and Bancroftian Filariasis. Microbiology and Immunology, 48, 519-525.
https://doi.org/10.1111/j.1348-0421.2004.tb03547.x
[3]
Bukau, B. (1993) Regulation of the Escherichia coli Heat-Shock Response. Molecular Microbiology, 9, 671-680. https://doi.org/10.1111/j.1365-2958.1993.tb01727.x
[4]
Cadavid Restrepo, A.M., Gass, K., Won, K.Y., Sheel, M., Robinson, K., Graves, P.M., Fuimaono, S. and Lau, C.L. (2022) Potential Use of Antibodies to Provide an Earlier Indication of Lymphatic Filariasis Resurgence in Post-Mass Drug Administration Surveillance in American Samoa. International Journal of Infectious Diseases, 117, 378-386. https://doi.org/10.1016/j.ijid.2022.02.006
[5]
Carrió, M.M. and Villaverde, A. (2005) Localization of Chaperones DnaK and GroEL in Bacterial Inclusion Bodies. Journal of Bacteriology, 187, 3599-3601.
https://doi.org/10.1128/JB.187.10.3599-3601.2005
[6]
Carter, J.V., Pan, J., Rai, S.N. and Galandiuk, S. (2016) ROC-ing along: Evaluation and Interpretation of Receiver Operating Characteristic Curves. Surgery (United States), 159, 1638-1645. https://doi.org/10.1016/j.surg.2015.12.029
[7]
Chandy, A., Thakur, A.S., Singh, M.P. and Manigauha, A. (2011) A Review of Neglected Tropical Diseases: Filariasis. Asian Pacific Journal of Tropical Medicine, 4, 581-586. https://doi.org/10.1016/S1995-7645(11)60150-8
[8]
Fujii, Y., Kaneko, S., Nzou, S. M., Mwau, M., Njenga, S.M., Tanigawa, C., Kimotho, J., Mwangi, A.W., Kiche, I. and Matsumoto, S. (2014) Serological Surveillance Development for Tropical Infectious Diseases Using Simultaneous Microsphere-Based Multiplex Assays and Finite Mixture Models. PLOS Neglected Tropical Diseases, 8, e3040. https://doi.org/10.1371/journal.pntd.0003040
[9]
Gan, S.D. and Patel, K.R. (2013) Enzyme Immunoassay and Enzyme-Linked Immunosorbent Assay. Journal of Investigative Dermatology, 133, 1-3.
https://doi.org/10.1038/jid.2013.287
[10]
Ganapathy, M., Chakravarthi, M., Charles, S.J., Harunipriya, P., Jaiganesh, S., Subramonian, N. and Kaliraj, P. (2015) Immunodiagnostic Properties of Wuchereria bancrofti SXP-1, a Potential Filarial Diagnostic Candidate Expressed in Tobacco Plant, Nicotiana tabacum. Applied Biochemistry and Biotechnology, 176, 1889-1903.
https://doi.org/10.1007/s12010-015-1685-0
[11]
Gass, K., de Rochars, M.V.E.B., Boakye, D., Bradley, M., Fischer, P.U., Gyapong, J., Itoh, M., Ituaso-Conway, N., Joseph, H., Kyelem, D., Laney, S.J., Legrand, A.M., Liyanage, T.S., Melrose, W., Mohammed, K., Pilotte, N., Ottesen, E.A., Plichart, C., Ramaiah, K. and Lammie, P. (2012) A Multicenter Evaluation of Diagnostic Tools to Define Endpoints for Programs to Eliminate Bancroftian Filariasis. PLOS Neglected Tropical Diseases, 6, e1479. https://doi.org/10.1371/journal.pntd.0001479
[12]
Gounoue-kamkumo, R., Nana-djeunga, H.C., Bopda, J., Akame, J., Tarini, A. and Kamgno, J. (2015) 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, 15, Article No. 579. https://doi.org/10.1186/s12879-015-1317-x
[13]
Houser, B. (2012) Bio-rad’s Bio-Plex® Suspension Array System, xMAP Technology Overview. Archives of Physiology and Biochemistry, 118, 192-196.
https://doi.org/10.3109/13813455.2012.705301
[14]
Irumva, V., Waihenya, R., Mwangi, A.W., Kipkemboi, P., Kaneko, S., Teya, T., Jepkemei, J., Njoroge, C., Gitari, J.W., Munyao, M.M., Irekwa, R.M., Ng’ang’a, M. and Nzou, S.M. (2019) Evaluation of the TbgI2 and TbgI17 Tandem Repeat Antigens as Potential Antigens for the Diagnosis of Trypanosoma brucei rhodesiense. Open Journal of Clinical Diagnostics, 9, 152-163. https://doi.org/10.4236/ojcd.2019.94011
[15]
Kubofcik, J., Fink, D.L. and Nutman, T.B. (2012) Identification of Wb123 as an Early and Specific Marker of Wuchereria bancrofti Infection. PLOS Neglected Tropical Diseases, 6, e1930. https://doi.org/10.1371/journal.pntd.0001930
[16]
Kumar, R. and Indrayan, A. (2011) Kumar-2011-Receiver Operating Characteristic 1. Indian Pediatrics, 48, 277-287. https://doi.org/10.1007/s13312-011-0055-4
[17]
Lammie, P.J., Weil, G., Noordin, R., Kaliraj, P., Steel, C., Goodman, D., Lakshmikanthan, V.B. and Ottensen, E. (2004) Recombinant Antigen-Based Antibody Assays for the Diagnosis and Surveillance of Lymphatic Filariasis—A Multicenter Trial. Filaria Journal, 3, Article No. 9. https://doi.org/10.1186/1475-2883-3-9
[18]
Malecela, M.N. and Ducker, C. (2021) A Road Map for Neglected Tropical Diseases 2021-2030. Transactions of the Royal Society of Tropical Medicine and Hygiene, 115, 121-123. https://doi.org/10.1093/trstmh/trab002
[19]
Mandrekar, J.N. (2010) Receiver Operating Characteristic Curve in Diagnostic Test Assessment. Journal of Thoracic Oncology, 5, 1315-1316.
https://doi.org/10.1097/JTO.0b013e3181ec173d
[20]
Nzou, S.M., Fujii, Y., Miura, M., Mwau, M., Mwangi, A. W., Itoh, M., Salam, M.A., Hamano, S., Hirayama, K. and Kaneko, S. (2016) Development of Multiplex Serological Assay for the Detection of Human African Trypanosomiasis. Parasitology International, 65, 121-127. https://doi.org/10.1016/j.parint.2015.10.008
[21]
Rahmah, N., Lim, B.H., Khairul Anuar, A., Shenoy, R.K., Kumaraswami, V., Lokman Hakim, S., Chotechuang, P., Kanjanopas, K. and Ramachandran, C.P. (2001) A Recombinant Antigen-Based IgG4 ELISA for the Specific and Sensitive Detection of Brugia malayi Infection. Transactions of the Royal Society of Tropical Medicine and Hygiene, 95, 280-284. https://doi.org/10.1016/S0035-9203(01)90234-2
[22]
Ramaiah, K.D., Das, P.K., Michael, E. and Guyatt, H.L. (2000) The Economic Burden of Lymphatic Filariasis in India. Parasitology Today, 16, 251-253.
https://doi.org/10.1016/S0169-4758(00)01643-4
[23]
Rao, K.V.N., Eswaran, M., Ravi, V., Gnanasekhar, B., Narayanan, R.B., Kaliraj, P., Jayaraman, K., Marson, A., Raghavan, N. and Scott, A.L. (2000) The Wuchereria bancrofti orthologue of Brugia malayi SXP1 and the Diagnosis of Bancroftian Filariasis. Molecular and Biochemical Parasitology, 107, 71-80.
https://doi.org/10.1016/S0166-6851(99)00231-5
[24]
Rebollo, M.P. and Bockarie, M.J. (2014) Shrinking the Lymphatic Filariasis Map: Update on Diagnostic Tools for Mapping and Transmission Monitoring. Parasitology, 141, 1912-1917. https://doi.org/10.1017/S0031182014001231
[25]
Restrepo, C., Gass, K., Won, K., Sheel, M., Robinson, K., Graves, P., Fuimaono, S. and Lau, C. (2022) Potential Use of Antibodies to Provide an Earlier Indication of Lymphatic Filariasis Resurgence in Post-Mass Drug Administration Surveillance in American Samoa. International Journal of Infectious Diseases, 117, 378-386.
https://doi.org/10.1016/j.ijid.2022.02.006
[26]
Sarr, J., Orlandi-Pradines, E., Fortin, S., Sow, C., Cornelie, S., Rogerie, F., Guindo, S., Konate, L., Fusa, T., Riveau, G., Rogier, C. and Remoue, F. (2011) Assessment of Exposure to Plasmodium falciparum Transmission in a Low Endemicity Area by Using Multiplex Fluorescent Microsphere-Based Serological Assays. Parasites and Vectors, 4, Article No. 212. https://doi.org/10.1186/1756-3305-4-212
[27]
Solomon, A.W., Engels, D., Bailey, R.L., Blake, I.M., Brooker, S., Chen, J.X., Chen, J.H., Churcher, T.S., Drakeley, C.J., Edwards, T., Fenwick, A., French, M., Gabrielli, A.F., Grassly, N.C., Harding-Esch, E.M., Holland, M.J., Koukounari, A., Lammie, P.J., Leslie, J. and Peeling, R.W. (2012) A Diagnostics Platform for the Integrated Mapping, Monitoring, and Surveillance of Neglected Tropical Diseases: Rationale and Target Product Profiles. PLOS Neglected Tropical Diseases, 6, e1746.
https://doi.org/10.1371/journal.pntd.0001746
[28]
Steel, C., Golden, A., Kubofcik, J., LaRue, N., De los Santos, T., Domingo, G.J. and Nutman, T.B. (2013) Rapid Wuchereria bancrofti-Specific Antigen Wb123-Based IgG4 Immunoassays as Tools for Surveillance Following Mass Drug Administration Programs on Lymphatic Filariasis. Clinical and Vaccine Immunology, 20, 1155-1161.
https://doi.org/10.1128/CVI.00252-13
[29]
Steel, C., Golden, A., Stevens, E., Yokobe, L., Domingo, G.J., De los Santos, T. and Nutman, T.B. (2015) Rapid Point-of-Contact Tool for Mapping and Integrated Surveillance of Wuchereria bancrofti and Onchocerca volvulus Infection. Clinical and Vaccine Immunology, 22, 896-901. https://doi.org/10.1128/CVI.00227-15
[30]
Tanigawa, C., Fujii, Y., Miura, M. and Nzou, S.M. (2015) Species-Specific Serological Detection for Schistosomiasis by Serine Protease Inhibitor (SERPIN) in Multiplex Assay. PLOS Neglected Tropical Diseases, 9, e0004021.
https://doi.org/10.1371/journal.pntd.0004021
[31]
Taylor, M.J., Hoerauf, A. and Bockarie, M. (2010) Lymphatic Filariasis and Onchocerciasis. The Lancet, 376, 1175-1185.
https://doi.org/10.1016/S0140-6736(10)60586-7
[32]
Janardhan, S., et al. (2007) Production, Purification and Diagnostic Application of Filarial Recombinant Protein WbSXP-1 Expressed in Salt Inducible Escherichia coli. Journal of Industrial Microbiology and Biotechnology, 34, 675-683.
https://doi.org/10.1007/s10295-007-0243-3
[33]
Tyrell, E. (2013) Socioeconomic Burden of Lymphatic Filariasis in Georgetown, Guyana. Tropical Medicine and International Health, 18, 152-158.
https://doi.org/10.1111/tmi.12017
[34]
Wanji, S., Amvongo-Adjia, N., Koudou, B., Njouendou, A.J., Chounna Ndongmo, P.W., Kengne-Ouafo, J.A., Datchoua-Poutcheu, F.R., Fovennso, B.A., Tayong, D.B., Fombad, F.F., Fischer, P.U., Enyong, P.I. and Bockarie, M. (2015) 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, 9, e0004184. https://doi.org/10.1371/journal.pntd.0004184
[35]
Wanji, S., Amvongo-Adjia, N., Njouendou, A.J., Kengne-Ouafo, J.A., Ndongmo, W. P.C., Fombad, F.F., Koudou, B., Enyong, P.A. and Bockarie, M. (2016) Further Evidence of the Cross-Reactivity of the Binax NOW® Filariasis ICT Cards to Non-Wuchereria bancrofti filariae: Experimental Studies with Loa loa and Onchocerca ochengi. Parasites and Vectors, 9, Article No. 267.
https://doi.org/10.1186/s13071-016-1556-8
[36]
Weil, G.J. and Ramzy, R.M.R. (2007) Diagnostic Tools for Filariasis Elimination Programs. Trends in Parasitology, 23, 78-82.
https://doi.org/10.1016/j.pt.2006.12.001
[37]
Won, K., Gass, K., Biamonte, M., Dagne, D.A., Ducker, C., Hanna, C., Hoerauf, A., Lammie, P., Njenga, S., Noordin, R., Ramaiah, K., Ramzy, R., Scholte, R.G.C., Solomon, A., Souza, A., Tappero, J., Toubali, E., Weil, G., Williams, S. and King, J. (2021) Diagnostics to Support Elimination of Lymphatic Filariasis-Development of Two Target Product Profiles. PLOS Neglected Tropical Diseases, 15, e0009968.
https://doi.org/10.1371/journal.pntd.0009968
[38]
Won, K., Sambou, S., Barry, A., Robinson, K., Jaye, M., Sanneh, B., Sanyang, A., Gass, K., Lammie, P. and Rebollo, M. (2018) Use of Antibody Tools to Provide Serologic Evidence of Elimination of Lymphatic Filariasis in the Gambia. American Journal of Tropical Medicine and Hygiene, 98, 15-20.
https://doi.org/10.4269/ajtmh.17-0371
[39]
World Health Organization (WHO) (n.d.) Control of Neglected Tropical Diseases.
https://www.who.int/teams/control-of-neglected-tropical-diseases/lymphatic-filariasis/diagnosis-and-treatment
[40]
World Health Organization (WHO) (n.d.) Lymphatic Filariasis.
https://www.who.int/news-room/fact-sheets/detail/lymphatic-filariasis
[41]
Zeldenryk, L.M., Gray, M., Speare, R., Gordon, S. and Melrose, W. (2011) The Emerging Story of Disability Associated with Lymphatic Filariasis: A Critical Review. PLOS Neglected Tropical Diseases, 5, e1366.
https://doi.org/10.1371/journal.pntd.0001366
