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Diagnostic application of sensitive and specific phage-exposed epitopes for visceral leishmaniasis and human immunodeficiency virus coinfection

Published online by Cambridge University Press:  19 August 2021

Fernanda F. Ramos ,
Grasiele S. V. Tavares ,
Fernanda Ludolf ,
Amanda S. Machado ,
Thaís T. O. Santos ,
Isabela A. P. Gonçalves ,
Ana C. S. Dias ,
Patrícia T. Alves ,
Vanessa G. Fraga  and
Raquel S. Bandeira
...Show all authors
Fernanda F. Ramos
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Grasiele S. V. Tavares
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Fernanda Ludolf
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Amanda S. Machado
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Thaís T. O. Santos
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Isabela A. P. Gonçalves
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Ana C. S. Dias
Affiliation:
Laboratório de Nanobiotecnologia, Instituto de Genética e Bioquímica, Universidade Federal de Uberlândia, Av. Amazonas s/n, Campus Umuarama, Bloco 2E, Sala 248, 38400-902 Uberlândia, Minas Gerais, Brazil
Patrícia T. Alves
Affiliation:
Laboratório de Nanobiotecnologia, Instituto de Genética e Bioquímica, Universidade Federal de Uberlândia, Av. Amazonas s/n, Campus Umuarama, Bloco 2E, Sala 248, 38400-902 Uberlândia, Minas Gerais, Brazil
Vanessa G. Fraga
Affiliation:
Laboratório de Nanobiotecnologia, Instituto de Genética e Bioquímica, Universidade Federal de Uberlândia, Av. Amazonas s/n, Campus Umuarama, Bloco 2E, Sala 248, 38400-902 Uberlândia, Minas Gerais, Brazil
Raquel S. Bandeira
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
João A. Oliveira-da-Silva
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Thiago A. R. Reis
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Daniela P. Lage
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Vívian T. Martins
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Camila S. Freitas
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Ana T. Chaves
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Nathalia S. Guimarães
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Miguel A. Chávez-Fumagalli
Affiliation:
Universidad Católica de Santa María, Urb. San José S/N, Umacollo, Arequipa, Peru
Unaí Tupinambás
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Manoel O. C. Rocha
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil
Gláucia F. Cota
Affiliation:
Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, FIOCRUZ, Belo Horizonte, Minas Gerais, Brazil
Ricardo T. Fujiwara
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, Minas Gerais, Brazil
Lílian L. Bueno
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte 31270-901, Minas Gerais, Brazil
Luiz Ricardo Goulart
Affiliation:
Laboratório de Nanobiotecnologia, Instituto de Genética e Bioquímica, Universidade Federal de Uberlândia, Av. Amazonas s/n, Campus Umuarama, Bloco 2E, Sala 248, 38400-902 Uberlândia, Minas Gerais, Brazil Department of Medical Microbiology and Immunology, University of California-Davis, Davis, CA 95616, USA
Eduardo A. F. Coelho*
Affiliation:
Programa de Pós-Graduação em Ciências da Saúde: Infectologia e Medicina Tropical, Faculdade de Medicina, Universidade Federal de Minas Gerais, Av. Prof. Alfredo Balena, 190, Belo Horizonte 30130-100, Minas Gerais, Brazil Departamento de Patologia Clínica, COLTEC, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Pampulha, Belo Horizonte 31270-901, Minas Gerais, Brazil
*
Author for correspondence: Eduardo A. F. Coelho, E-mail: [email protected]
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Abstract

The diagnosis of visceral leishmaniasis (VL) has improved with the search of novel antigens; however, their performance is limited when samples from VL/human immunodeficiency virus (HIV)-coinfected patients are tested. In this context, studies conducted to identify more suitable antigens to detect both VL and VL/HIC coinfection cases should be performed. In the current study, phage display was performed using serum samples from healthy subjects and VL, HIV-infected and VL/HIV-coinfected patients; aiming to identify novel phage-exposed epitopes to be evaluated with this diagnostic purpose. Nine non-repetitive and valid sequences were identified, synthetized and tested as peptides in enzyme-linked immunosorbent assay experiments. Results showed that three (Pep2, Pep3 and Pep4) peptides showed excellent performance to diagnose VL and VL/HIV coinfection, with 100% sensitivity and specificity values. The other peptides showed sensitivity varying from 50.9 to 80.0%, as well as specificity ranging from 60.0 to 95.6%. Pep2, Pep3 and Pep4 also showed a potential prognostic effect, since specific serological reactivity was significantly decreased after patient treatment. Bioinformatics assays indicated that Leishmania trypanothione reductase protein was predicted to contain these three conformational epitopes. In conclusion, data suggest that Pep2, Pep3 and Pep4 could be tested for the diagnosis of VL and VL/HIV coinfection.

Keywords

Diagnosishuman immunodeficiency virusphage displaytrypanothione reductasevisceral leishmaniasisVL/HIV coinfection
Type
Research Article
Information
Parasitology , Volume 148 , Issue 13 , November 2021 , pp. 1706 - 1714
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

Co-senior authors of this work.

References

Alfaleh, MA, Alsaab, HO, Mahmoud, AB, Alkayyal, AA, Jones, ML, Mahler, SM and Hashem, AM (2020) Phage display derived monoclonal antibodies: from bench to bedside. Frontiers in Immunology 11, 1986.CrossRefGoogle ScholarPubMed
Almagro, JC, Pedraza-Escalona, M, Arrieta, HI and Pérez-Tapia, SM (2019) Phage display libraries for antibody therapeutic discovery and development. Antibodies (Basel) 8, 44.CrossRefGoogle ScholarPubMed
Alvar, J, Aparicio, P, Aseffa, A, Den Boer, M, Cañavate, C, Dedet, JP, Gradoni, L, Ter Horst, R, López-Vélez, R and Moreno, J (2008) The relationship between leishmaniasis and AIDS: the second 10 years. Clinical Microbiology Reviews 21, 334–359.CrossRefGoogle ScholarPubMed
Alves, PT, Fujimura, PT, Morais, LD and Goulart, LR (2014) Revisiting the CD14: epitope mapping by phage display. Immunobiology 219, 822–829.CrossRefGoogle ScholarPubMed
Battista, T, Colotti, G, Ilari, A and Fiorillo, A (2020) Targeting trypanothione reductase, a key enzyme in the redox trypanosomatid metabolism, to develop new drugs against leishmaniasis and trypanosomiases. Molecules 25, 1924.CrossRefGoogle ScholarPubMed
Beig, M, Oellien, F, Garo, L, Noack, S, Krauth-Siegel, RL and Selzer, PM (2015) Trypanothione reductase: a target protein for a combined in vitro and in silico screening approach. PLoS Neglected Tropical Diseases 9, e0003773.CrossRefGoogle ScholarPubMed
Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Carvalho, AMRS, Mendes, TAO, Coelho, EAF, Duarte, MC and Menezes-Souza, D (2018) New antigens for the serological diagnosis of human visceral leishmaniasis identified by immunogenomic screening. PLoS One 13, e0209599.CrossRefGoogle ScholarPubMed
Carvalho, GB, Costa, LE, Lage, DP, Ramos, FF, Santos, TTO, Ribeiro, PAF, Dias, DS, Salles, BCS, Lima, MP, Carvalho, LM, Dias, ACS, Alves, PT, Franklin, ML, Silva, RAM, Duarte, MC, Menezes-Souza, D, Roatt, BM, Chávez-Fumagalli, MA, Goulart, LR, Teixeira, AL and Coelho, EAF (2019) High-through identification of T cell-specific phage-exposed mimotopes using PBMCs from tegumentary leishmaniasis patients and their use as vaccine candidates against Leishmania amazonensis infection. Parasitology 146, 322–332.CrossRefGoogle Scholar
Coelho, EAF, Tavares, CA, Carvalho, FA, Chaves, KF, Teixeira, KN, Rodrigues, RC, Charest, H, Matlashewski, G, Gazzinelli, RT and Fernandes, AP (2003) Immune responses induced by the Leishmania (Leishmania) donovani A2 antigen, but not by the LACK antigen, are protective against experimental Leishmania (Leishmania) amazonensis infection. Infection and Immunity 71, 3988–3994.CrossRefGoogle Scholar
Costa, MM, Penido, M, Santos, MS, Doro, D, Freitas, E, Michalick, MS, Grimaldi, G, Gazzinelli, RT and Fernandes, AP (2012) Improved canine and human visceral leishmaniasis immunodiagnosis using combinations of synthetic peptides in enzyme-linked immunosorbent assay. PLoS Neglected Tropical Diseases 6, e1622.CrossRefGoogle ScholarPubMed
Costa, LE, Lima, MIS, Chávez-Fumagalli, MA, Menezes-Souza, D, Martins, VT, Duarte, MC, Lage, PS, Lopes, EGP, Lage, DP, Ribeiro, TG, Andrade, PHR, Magalhães-Soares, DF, Soto, M, Tavares, CAP, Goulart, LR and Coelho, EAF (2014) Subtractive phage display selection from canine visceral leishmaniasis identifies novel epitopes that mimic Leishmania infantum antigens with potential serodiagnosis applications. Clinical and Vaccine Immunology 21, 96–106.CrossRefGoogle ScholarPubMed
Costa, LE, Chávez-Fumagalli, MA, Martins, VT, Duarte, MC, Lage, DP, Lima, MI, Pereira, NC, Soto, M, Tavares, CA, Goulart, LR and Coelho, EA (2015) Phage-fused epitopes from Leishmania infantum used as immunogenic vaccines confer partial protection against Leishmania amazonensis infection. Parasitology 42, 1335–1347.CrossRefGoogle Scholar
Costa, LE, Salles, BCS, Santos, TTO, Ramos, FF, Lima, MP, Lima, MIS, Portela, ÁSB, Chávez-Fumagalli, MA, Duarte, MC, Menezes-Souza, D, Machado-de-Ávila, RA, Silveira, JAG, Magalhães-Soares, DF, Goulart, LR and Coelho, EAF (2017) Antigenicity of phage clones and their synthetic peptides for the serodiagnosis of canine and human visceral leishmaniasis. Microbial Pathogenesis 110, 14–22.CrossRefGoogle ScholarPubMed
Cota, GF, Sousa, MR and Rabello, A (2011) Predictors of visceral leishmaniasis relapse in HIV-infected patients: a systematic review. PLoS Neglected Tropical Diseases 5, e1153.CrossRefGoogle ScholarPubMed
Cota, GF, Sousa, MR, Demarqui, FN and Rabello, A (2012) The diagnostic accuracy of serologic and molecular methods for detecting visceral leishmaniasis in HIV-infected patients: meta-analysis. PLoS Neglected Tropical Diseases 6, e1665.CrossRefGoogle ScholarPubMed
Cota, GF, Sousa, MR, Nogueira, BMF, Gomes, LI, Oliveira, E, Assis, TS, Mendonça, AL, Pinto, BF, Saliba, JW and Rabello, A (2013) Comparison of parasitological, serological, and molecular tests for visceral leishmaniasis in HIV-infected patients: a cross-sectional delayed-type study. American Journal of Tropical Medicine and Hygiene 89, 570–577.CrossRefGoogle ScholarPubMed
Coutinho, JVSC, Santos, FSD, Ribeiro, RDSP, Oliveira, IBB, Dantas, VB, Santos, ABFS and Tauhata, JR (2017) Visceral leishmaniasis and leishmaniasis-HIV coinfection: comparative study. Revista da Sociedade Brasileira de Medicina Tropical 50, 670–674.CrossRefGoogle ScholarPubMed
Ejazi, SA, Bhattacharyya, A, Choudhury, ST, Ghosh, S, Sabur, A, Pandey, K, Das, VNR, Das, P, Rahaman, M, Goswami, RP and Ali, N (2018) Immunoproteomic identification and characterization of Leishmania membrane proteins as non-invasive diagnostic candidates for clinical visceral leishmaniasis. Scientific Reports 8, 12110.CrossRefGoogle ScholarPubMed
Fargeas, C, Hommel, M, Maingon, R, Dourado, C, Monsigny, M and Mayer, R (1996) Synthetic peptide-based enzyme-linked immunosorbent assay for serodiagnosis of visceral leishmaniasis. Journal of Clinical Microbiology 34, 241–248.CrossRefGoogle ScholarPubMed
Faria, AR, Veloso, LC, Coura-Vital, W, Reis, AB, Damasceno, LM, Gazzinelli, RT and Andrade, HM (2015) Novel recombinant multiepitope proteins for the diagnosis of asymptomatic Leishmania infantum-infected dogs. PLoS Neglected Tropical Diseases 9, e3429.CrossRefGoogle Scholar
Gazarian, K, Rowlay, M, Gazarian, T, Vazquez-Buchelli, JE and Hernández-Gonzáles, M (2012) Mimotope peptides selected from phage display combinatorial library by serum antibodies of pigs experimentally infected with Taenia solium as leads to developing diagnostic antigens for human neurocysticercosis. Peptides 38, 381–388.CrossRefGoogle ScholarPubMed
Holloway, GA, Charman, WN, Fairlamb, AH, Brun, R, Kaiser, M, Kostewicz, E, Novello, PM, Parisot, JP, Richardson, J, Street, IP, Watson, KG and Baell, JB (2009) Trypanothione reductase high-throughput screening campaign identifies novel classes of inhibitors with antiparasitic activity. Antimicrobial and Agents Chemotherapy 53, 2824–2833.CrossRefGoogle ScholarPubMed
Ilari, A, Genovese, I, Fiorillo, F, Battista, T, De Ionna, I, Fiorillo, A and Colotti, G (2018) Toward a drug against all Kinetoplastids: from Leishbox to specific and potent trypanothione reductase inhibitors. Molecular Pharmacology 15, 3069–3078.CrossRefGoogle Scholar
Kassa, M, Abdellati, S, Cnops, L, Bremer-Hinckel, BC, Yeshanew, A, Hailemichael, W, Vogt, F, Adriaensen, W, Mertens, P, Diro, E, Van Griensven, J and Van den Bossche, D (2020) Diagnostic accuracy of direct agglutination test, rK39 ELISA and six rapid diagnostic tests among visceral leishmaniasis patients with and without HIV coinfection in Ethiopia. PLoS Neglected Tropical Diseases 14, e0008963.CrossRefGoogle ScholarPubMed
Kaye, PM, Cruz, I, Picado, A, Van Bocxlaer, K and Croft, SL (2020) Leishmaniasis immunopathology-impact on design and use of vaccines, diagnostics and drugs. Seminars in Immunopathology 42, 247–264.CrossRefGoogle ScholarPubMed
Kuhn, P, Fühner, V, Unkauf, T, Moreira, GM, Frenzel, A, Miethe, S and Hust, M (2016) Recombinant antibodies for diagnostics and therapy against pathogens and toxins generated by phage display. Proteomics – Clinical Applications 10, 922–948.CrossRefGoogle ScholarPubMed
Kumar, P, Pai, K, Tripathi, K, Pandey, HP and Sundar, S (2002) Immunoblot analysis of the humoral immune response to Leishmania donovani polypeptides in cases of human visceral leishmaniasis: its usefulness in prognosis. Clinical and Diagnostic Laboratory Immunology 9, 1119–1123.Google ScholarPubMed
Lindoso, JAL, Moreira, CHV, Cunha, MA and Queiroz, IT (2018) Visceral leishmaniasis and HIV coinfection: current perspectives. HIV AIDS (Auckland) 10, 193–201.Google ScholarPubMed
Link, JS, Alban, SM, Soccol, CR, Pereira, GV and Soccol, VT (2017) Synthetic peptides as potential antigens for cutaneous leishmaniosis diagnosis. Journal of Immunological Research 2017, 5871043.CrossRefGoogle ScholarPubMed
Luz, JGG, Naves, DB, Carvalho, AG, Meira, GA, Dias, JVL and Fontes, CJF (2018) Visceral leishmaniasis in a Brazilian endemic area: an overview of occurrence, HIV coinfection and lethality. Revista do Instituto de Medicina Tropical de São Paulo 60, e12.CrossRefGoogle Scholar
Machado, AS, Ramos, FF, Oliveira-da-Silva, JA, Santos, TTO, Ludolf, F, Tavares, GSV, Costa, LE, Lage, DP, Steiner, BT, Chaves, AT, Chávez-Fumagalli, MA, Magalhães-Soares, DF, Silveira, JAG, Napoles, KMN, Tupinambás, U, Duarte, MC, Machado-de-Ávila, RA, Bueno, LL, Fujiwara, RT, Moreira, RLF, Rocha, MOC, Caligiorne, RB and Coelho, EAF (2020) A Leishmania infantum hypothetical protein evaluated as a recombinant protein and specific B-cell epitope for the serodiagnosis and prognosis of visceral leishmaniasis. Acta Tropica 203, 105318.CrossRefGoogle ScholarPubMed
Manoutcharian, K (2005) Bacteriophages as tools for vaccine and drug development. Expert Review of Vaccines 4, 5–7.CrossRefGoogle Scholar
Meloen, RH, Puijk, WC, Langeveld, JP, Langedijk, JP and Timmerman, P (2003) Design of synthetic peptides for diagnostics. Current Protein & Peptide Science 4, 253–260.CrossRefGoogle ScholarPubMed
Ponte-Sucre, A, Gamarro, F, Dujardin, JC, Barrett, MP, López-Vélez, R, García-Hernández, R, Pountain, AW, Mwenechanya, R and Papadopoulou, B (2017) Drug resistance and treatment failure in leishmaniasis: a 21st century challenge. PLoS Neglected Tropical Diseases 11, e0006052.CrossRefGoogle ScholarPubMed
Rodrigues, MR, Santos, LMO, Miyazaki, CK, Martins, VT, Ludolf, FR, Kursancew, AC, Ramos, FF, Dias, DS, Oliveira, JS, Vieira, PMA, Roatt, BM, Machado-de-Ávila, RA, Gonçalves, DU, Menezes-Souza, D, Coelho, EAF and Duarte, MC (2019) Immunodiagnosis of human and canine visceral leishmaniasis using recombinant Leishmania infantum prohibitin protein and a synthetic peptide containing its conformational B-cell epitope. Journal of Immunological Methods 474, 112641.CrossRefGoogle Scholar
Ruiter, CM, Van Der Veer, C, Leeflang, MM, Deborggraeve, S, Lucas, C and Adams, ER (2014) Molecular tools for diagnosis of visceral leishmaniasis: systematic review and meta-analysis of diagnostic test accuracy. Journal of Clinical Microbiology 52, 3147–3155.CrossRefGoogle ScholarPubMed
Sakkas, H, Gartzonika, C and Levidiotou, S (2016) Laboratory diagnosis of human visceral leishmaniasis. Journal of Vector Borne Diseases 53, 8–16.Google ScholarPubMed
Santos-Gomes, G, Gomes-Pereira, S, Campino, L, Araújo, MD and Abranches, P (2000) Performance of immunoblotting in diagnosis of visceral Leishmaniasis in human immunodeficiency virus-Leishmania sp.-coinfected patients. Journal of Clinical Microbiology 38, 175–178.CrossRefGoogle ScholarPubMed
Silva, MRB, Brandão, NAA, Colovati, M, Sousa, MMP, Lima, LC, Dorta, ML, Ribeiro-Dias, F, Costa, DL, Costa, CHN and Oliveira, MAP (2018) Performance of two immunochromatographic tests for diagnosis of visceral leishmaniasis in patients coinfected with HIV. Parasitology Research 117, 419–427.CrossRefGoogle ScholarPubMed
Srivastava, S, Shankar, P, Mishra, J and Singh, S (2016) Possibilities and challenges for developing a successful vaccine for leishmaniasis. Parasite & Vectors 9, 277.CrossRefGoogle ScholarPubMed
Srividya, G, Kulshrestha, A, Singh, R and Salotra, P (2012) Diagnosis of visceral leishmaniasis: developments over the last decade. Parasitology Research 110, 1065–1078.CrossRefGoogle ScholarPubMed
Tajebe, F, Getahun, M, Adem, E, Hailu, A, Lemma, M, Fikre, H, Raynes, J, Tamiru, A, Mulugeta, Z, Diro, E, Toulza, F, Shkedy, Z, Ayele, T, Modolell, M, Munder, M, Müller, I, Takele, Y and Kropf, P (2017) Disease severity in patients with visceral leishmaniasis is not altered by co-infection with intestinal parasites. PLoS Neglected Tropical Diseases 11, e0005727.CrossRefGoogle Scholar
Thakur, S, Joshi, J and Kaur, S (2020) Leishmaniasis diagnosis: an update on the use of parasitological, immunological and molecular methods. Journal of Parasitic Diseases 44, 1–20.CrossRefGoogle ScholarPubMed
Toledo-Machado, CM, Avila, RA, Nguyen, C, Granier, C, Bueno, LL, Carneiro, CM, Menezes-Souza, D, Carneiro, RA, Chávez-Olórtegui, C and Fujiwara, RT (2015 a) Immunodiagnosis of canine visceral leishmaniasis using mimotope peptides selected from phage displayed combinatorial libraries. BioMed Research International 2015, 401509.CrossRefGoogle ScholarPubMed
Toledo-Machado, CM, Bueno, LL, Menezes-Souza, D, Machado-de-Avila, RA, Nguyen, C, Granier, C, Bartholomeu, DC, Chávez-Olórtegui, C and Fujiwara, RT (2015 b) Use of phage display technology in development of canine visceral leishmaniasis vaccine using synthetic peptide trapped in sphingomyelin/cholesterol liposomes. Parasite & Vectors 8, 133.CrossRefGoogle ScholarPubMed
Torres-Guerrero, E, Quintanilla-Cedillo, MR, Ruiz-Esmenjaud, J and Arenas, R (2017) Leishmaniasis: a review. F1000 Research 6, 750.CrossRefGoogle ScholarPubMed
World Health Organization (2018) Leishmaniasis. See http://www.who.int/topics/leishmaniasis/en/.Google Scholar
Xin, L, Jinyan, G, Shengfa, H, Yuanyuan, W and Hongbing, C (2014) Identification of conformational antigenic epitopes and dominant amino acids of buffalo β-lactoglobulin. Journal of Food Science 79, T748–T756.CrossRefGoogle ScholarPubMed