From infection to vaccination: reviewing the global burden, history of vaccine development, and recurring challenges in global leishmaniasis protection

References

• Organization WH. Investing to overcome the global impact of neglected tropical diseases: third WHO report on neglected tropical diseases (World Health Organization, Geneva, 2015).
   Google Scholar
• Maroli M, Feliciangeli Md, Bichaud L, et al. Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med Vet Entomol. 2013;27(2):123–147.
   PubMed Web of Science ®Google Scholar
• Kima PE. The amastigote forms of Leishmania are experts at exploiting host cell processes to establish infection and persist. Int J Parasitol. 2007;37(10):1087–1096.
   PubMed Web of Science ®Google Scholar
• Desjeux P. Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis. 2004;27(5):305–318.
   PubMed Web of Science ®Google Scholar
• Wilhelm TJ,Visceral leishmaniasis. Der Chirurg. 2019;90(10):833–837.
   PubMed Web of Science ®Google Scholar
• Pennisi MG, Persichetti MF. Feline leishmaniosis: is the cat a small dog? Vet Parasitol. 2018;251:131–137.
   PubMed Web of Science ®Google Scholar
• Mhadhbi M, Sassi A. Infection of the equine population by Leishmania parasites. Equine Vet J. 2020;52(1):28–33.
   PubMed Web of Science ®Google Scholar
• Han S, Wu W-P, Chen K, et al. Epidemiological survey of sheep as potential hosts for Leishmania in China. BMC Vet Res. 2018;14(1):378.
   PubMed Web of Science ®Google Scholar
• Pareyn M, Hendrickx R, Girma N, et al. Evaluation of a pan-Leishmania SL RNA qPCR assay for parasite detection in laboratory-reared and field-collected sand flies and reservoir hosts. Parasit Vectors. 2020;13(1). DOI:https://doi.org/10.1186/s13071-020-04141-y.
   Google Scholar
• Chen H, Li J, Zhang J, et al. Multi-locus characterization and phylogenetic inference of Leishmania spp. in snakes from Northwest China. PLoS ONE. 2019;14(4).
   Web of Science ®Google Scholar
• Zhang J-R, Guo X-G, Liu J-L, et al. Molecular detection, identification and phylogenetic inference of Leishmania spp. in some desert lizards from Northwest China by using internal transcribed spacer 1 (ITS1) sequences. Acta Trop. 2016;162:83–94.
   PubMed Web of Science ®Google Scholar
• Ashford RW. Leishmaniasis reservoirs and their significance in control. Clin Dermatol. 1996;14(5):523–532.
   PubMed Web of Science ®Google Scholar
• Tomassone L, Berriatua E, De Sousa R, et al. Neglected vector-borne zoonoses in Europe: into the wild. Vet Parasitol. 2018;251:17–26.
   PubMed Web of Science ®Google Scholar
• Tabbabi A. Review of Leishmaniasis in the Middle East and North Africa. Afr Health Sci. 2019;19(1):1329–1337.
   PubMed Web of Science ®Google Scholar
• Ghawar W, Bettaieb J, Salem S, et al. Natural infection of Ctenodactylus gundi by Leishmania major in Tunisia. Acta Trop. 2018;177:89–93.
   PubMed Web of Science ®Google Scholar
• Franco AO, Davies CR, Mylne A, et al. Predicting the distribution of canine leishmaniasis in western Europe based on environmental variables. Parasitology. 2011;138(14):1878–1891.
   PubMed Web of Science ®Google Scholar
• Miguel DC, Gaurnier DC. Canine and Human Leishmaniasis: disease progression to Brazilian Urbanized areas. 2019 2(3); International Journal of Tropical Diseases.
   Google Scholar
• Dantas-Torres F, Brandão-Filho SP. Visceral leishmaniasis in Brazil: revisiting paradigms of epidemiology and control. Rev Inst Med Trop Sao Paulo. 2006;48(3):151–156.
   PubMedGoogle Scholar
• Gurel MS, Tekin B, Uzun S. Cutaneous leishmaniasis: a great imitator. Clin Dermatol. 2020;38(2):140–151.
   PubMed Web of Science ®Google Scholar
• Akilov O, Khachemoune A, Hasan T. Clinical manifestations and classification of old World cutaneous leishmaniasis. Int J Dermatol. 2007;46(2):132–142.
   PubMed Web of Science ®Google Scholar
• Volpedo G, Pacheco-Fernandez T, Holcomb EA, et al. Mechanisms of immunopathogenesis in Cutaneous Leishmaniasis and Post Kala-azar Dermal Leishmaniasis (PKDL). Front Cell Infect Microbiol. 2021;11. DOI:https://doi.org/10.3389/fcimb.2021.685296
   Google Scholar
• Handler MZ, Patel PA, Kapila R, et al. Cutaneous and mucocutaneous leishmaniasis: differential diagnosis, diagnosis, histopathology, and management. J Am Acad Dermatol. 2015;73(6):911–926.
   PubMed Web of Science ®Google Scholar
• Srivastava P, Dayama A, Mehrotra S, et al. Diagnosis of visceral leishmaniasis. Trans R Soc Trop Med Hyg. 2011;105(1):1–6.
   PubMed Web of Science ®Google Scholar
• Vega-López F. Diagnosis of cutaneous leishmaniasis. Curr Opin Infect Dis. 2003;16(2):97–101.
   PubMed Web of Science ®Google Scholar
• Sundar S, Singh OP. Molecular diagnosis of Visceral Leishmaniasis. Mol Diagn Ther. 2018;22(4):443–457.
   PubMed Web of Science ®Google Scholar
• Thakur S, Joshi J, Kaur S. Leishmaniasis diagnosis: an update on the use of parasitological, immunological and molecular methods. J Parasitic Dis. 2020;44(2):253–272.
   PubMedGoogle Scholar
• Van Griensven J, Visceral Leishmaniasis: DE. Recent advances in diagnostics and treatment regimens. Infect Dis Clin North Am. 2019;33(1):79–99.
   PubMed Web of Science ®Google Scholar
• Moreira OC, Yadon ZE, Cupolillo E. The applicability of real-time PCR in the diagnostic of cutaneous leishmaniasis and parasite quantification for clinical management: current status and perspectives. Acta Trop. 2018;184:29–37.
   PubMed Web of Science ®Google Scholar
• Aronson NE, Joya CA, LeishmaniasisCutaneous Leishmaniasis: Updates in Diagnosis and Management. Infect Dis Clin North Am. 2019;33(1):101–117.
   PubMed Web of Science ®Google Scholar
• Rosenthal E, Marty P. Recent understanding in the treatment of visceral leishmaniasis. J Postgrad Med. 2003;49(1):61.
   PubMedGoogle Scholar
• Sundar S, More DK, Singh MK, et al. Failure of Pentavalent Antimony in Visceral Leishmaniasis in India: report from the center of the Indian Epidemic. Clinl Infect Dis. 2000;31(4):1104–1107.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Cutaneous Leishmaniasis control in selected countries of the two eastern Mediterranean and African regions. 2015. Geneva, Switzerland: World Health Organization
   Google Scholar
• Shirzadi MR. Lipsosomal amphotericin B: a review of its properties, function, and use for treatment of cutaneous leishmaniasis. Res Rep Trop Med. 2019;10:11–18.
   PubMed Web of Science ®Google Scholar
• Azab AS, Kamal MS, Haggar MSE, et al. Early surgical treatment of Cutaneous Leishmaniasis. The Journal of Dermatologic Surgery and Oncology. 1983;9(12):1007–1012.
   PubMedGoogle Scholar
• Bassiouny A, Meshad ME, Talaat M, et al. Cryosurgery in cutaneous leishmaniasis. Br J Dermatol. 1982;107(4):467–474.
   PubMed Web of Science ®Google Scholar
• Panagiotopoulos A, Stavropoulos PG, Hasapi V, et al. Treatment of cutaneous leishmaniasis with cryosurgery. Int J Dermatol. 2005;44(9):749–752.
   PubMed Web of Science ®Google Scholar
• Aronson NE, Wortmann GW, Byrne WR, et al. A randomized controlled trial of local heat therapy versus intravenous sodium stibogluconate for the treatment of cutaneous Leishmania major Infection. PLoS Negl Trop Dis. 2010;4(3):e628.
   PubMed Web of Science ®Google Scholar
• Bumb RA, Satoskar AR. Radiofrequency-induced heat therapy as first-line treatment for cutaneous leishmaniasis. Expert Rev Anti Infect Ther. 2011;9(6):623–625.
   PubMed Web of Science ®Google Scholar
• David JR. The successful use of radiofrequency-induced heat therapy for cutaneous leishmaniasis: a review. Parasitology. 2018;145(4):527–536.
   PubMed Web of Science ®Google Scholar
• Frolich S, Kaplan I. Plastic surgery in the treatment of Cutaneous Leishmaniasis of the face. Plast Reconstr Surg. 1967;40(2):157–160.
   PubMed Web of Science ®Google Scholar
• Rodrigues V, Cordeiro-da-Silva A, Laforge M, et al. Regulation of immunity during visceral Leishmania infection. Parasit Vectors. 2016;9:118. DOI:https://doi.org/10.1186/s13071-016-1412-x
   Google Scholar
• Pacheco-Fernandez T, Volpedo G, Verma C, et al. Understanding the immune responses involved in mediating protection or immunopathology during leishmaniasis. Biochem Soc Trans. 2021;49(1):297–311.
   PubMed Web of Science ®Google Scholar
• Nylén S, Gautam S. Immunological perspectives of leishmaniasis. J Glob Infect Dis. 2010;2(2):135–146.
   PubMedGoogle Scholar
• Sharma U, Singh S. Immunobiology of leishmaniasis. In: IJEB Vol.47(06) [June 2009]. Indian Journal of Experimental Biology. 2009.
   Google Scholar
• Kaye PM, Aebischer T. Visceral leishmaniasis: immunology and prospects for a vaccine. Clin Microbiol Infect. 2011;17(10):1462–1470.
   PubMed Web of Science ®Google Scholar
• Kaye PM, Svensson M, Ato M, et al. The immunopathology of experimental visceral leishmaniasis. Immunol Rev. 2004;201(1):239–253.
   PubMed Web of Science ®Google Scholar
• Scott P, Novais FO. Cutaneous leishmaniasis: immune responses in protection and pathogenesis. Nat Rev Immunol. 2016;16(9):581–592.
   PubMed Web of Science ®Google Scholar
• Real F, Florentino PTV, Reis LC, et al. Cell-to-cell transfer of Leishmania amazonensis amastigotes is mediated by immunomodulatory LAMP-rich parasitophorous extrusions. Cell Microbiol. 2014;16(10):1549–1564.
   PubMed Web of Science ®Google Scholar
• Hohman LS, Peters NC. CD4+ T Cell-Mediated Immunity against the Phagosomal Pathogen Leishmania: implications for Vaccination. Trends Parasitol. 2019;35(6):423–435.
   PubMed Web of Science ®Google Scholar
• Glennie ND, Volk SW, Skin-resident SP. CD4+ T cells protect against Leishmania major by recruiting and activating inflammatory monocytes. PLoS Pathog. 2017;13(4):e1006349.
   PubMed Web of Science ®Google Scholar
• Qadoumi M, Becker I, Donhauser N, et al. Expression of inducible nitric oxide synthase in skin lesions of patients with American Cutaneous Leishmaniasis | infection and immunity. ASM Journals Infection and Immunity. 2020 70(8).
   Google Scholar
• Á G, Valério-Bolas A, Palma-Marques J, et al. Cutaneous Leishmaniasis: the complexity of host’s effective immune response against a polymorphic parasitic disease. J Immunol Res. 2019;2019.
   Web of Science ®Google Scholar
• Bhor R, Rafati S, Pai K. Cytokine saga in visceral leishmaniasis. Cytokine. 2020;155322. DOI:https://doi.org/10.1016/j.cyto.2020.155322
   Google Scholar
• Alexander J, Carter KC, Al-Fasi N, et al. IL-4 is necessary for effective drug therapy against visceral leishmaniasis. Eur J Immunol. 2000;30(10):2935–2943.
   PubMed Web of Science ®Google Scholar
• Goto H, Lindoso J. Immunity and immunosuppression in experimental visceral leishmaniasis. Braz J Med Biol Res. 2004;37(4):615–623.
   PubMed Web of Science ®Google Scholar
• Rossi M, Fasel N. How to master the host immune system? Leishmania parasites have the solutions! Int Immunol. 2017;30(3):103–111.
   Web of Science ®Google Scholar
• Silveira FT, Lainson R, De Castro Gomes CM, et al. Immunopathogenic competences of Leishmania (V.) braziliensis and L. (L.) amazonensis in American cutaneous leishmaniasis. Parasite Immunol. 2009;31(8):423–431.
   PubMed Web of Science ®Google Scholar
• Srivastava P, Gidwani K, Picado A, et al. Molecular and serological markers of Leishmania donovani infection in healthy individuals from endemic areas of Bihar, India. Trop Med Int Health. 2013;18(5):548–554.
   PubMed Web of Science ®Google Scholar
• Nweze JA, Nweze EI, Onoja US. Nutrition, malnutrition, and leishmaniasis. Nutrition. 2020;73:110712.
   PubMed Web of Science ®Google Scholar
• Akuffo H, Costa C, Van Griensven J, et al. New insights into leishmaniasis in the immunosuppressed. PLoS Negl Trop Dis. 2018;12(5):e0006375.
   PubMed Web of Science ®Google Scholar
• Sakthianandeswaren A, Foote SJ, Handman E. The role of host genetics in leishmaniasis. Trends Parasitol. 2009;25(8):383–391.
   PubMed Web of Science ®Google Scholar
• Van Griensven J, Carrillo E, López-Vélez R, et al. Leishmaniasis in immunosuppressed individuals. Clin Microbiol Infect. 2014;20(4):286–299.
   PubMed Web of Science ®Google Scholar
• Monge-Maillo B, Norman FF, Cruz I, et al. Visceral Leishmaniasis and HIV Coinfection in the mediterranean region. PLoS Negl Trop Dis. 2014;8(8):e3021. doi: https://doi.org/10.1371/journal.pntd.0003021
   Google Scholar
• Malafaia G. Protein-energy malnutrition as a risk factor for visceral leishmaniasis: a review. Parasite Immunol. 2009;31(10):587–596.
   PubMed Web of Science ®Google Scholar
• Cuypers B, Berg M, Imamura H, et al. Integrated genomic and metabolomic profiling of ISC1, an emerging Leishmania donovani population in the Indian subcontinent. Infect Genet Evol. 2018;62:170–178.
   PubMed Web of Science ®Google Scholar
• Urrea DA, Duitama J, Imamura H, et al. Genomic analysis of Colombian Leishmania panamensis strains with different level of virulence. Sci Rep. 2018;8(1):17336.
   PubMed Web of Science ®Google Scholar
• Samarasinghe SR, Samaranayake N, Kariyawasam UL, et al. Genomic insights into virulence mechanisms of Leishmania donovani: evidence from an atypical strain. BMC Genomics. 2018;19(1):843.
   PubMed Web of Science ®Google Scholar
• Yasur-Landau D, Jaffe CL, David L, et al. Resistance of Leishmania infantum to allopurinol is associated with chromosome and gene copy number variations including decrease in the S-adenosylmethionine synthetase (METK) gene copy number. Int J Parasitol Drugs Drug Resist. 2018;8(3):403–410.
   PubMed Web of Science ®Google Scholar
• Sterkers Y, Crobu L, Lachaud L, et al. Parasexuality and mosaic aneuploidy in Leishmania: alternative genetics. Trends Parasitol. 2014;30(9):429–435.
   PubMed Web of Science ®Google Scholar
• Rougeron V, De Meeûs T, Bañuls AL. Reproduction in Leishmania: a focus on genetic exchange. Infect Genet Evol. 2017;50:128–132.
   PubMed Web of Science ®Google Scholar
• Telittchenko R, Descoteaux A. Study on the occurrence of genetic exchange among parasites of the Leishmania mexicana complex. Front Cell Infect Microbiol. 2020;10(607253). DOI:https://doi.org/10.3389/fcimb.2020.607253
   Google Scholar
• Romano A, Inbar E, Debrabant A, et al. Cross-species genetic exchange between visceral and cutaneous strains of Leishmania in the sand fly vector. Proc Natl Acad Sci U S A. 2014;111(47):16808–16813.
   PubMed Web of Science ®Google Scholar
• World Health Organization. 2016. Weekly epidemiological record. (Ed.^(Eds). 421–432.
   Google Scholar
• World Health Organization. Leishmaniasis, status of endemicity of cutaneous leishmaniasis: 2019. (Ed.^(Eds) (2019)
   Google Scholar
• World Health Organization. Leishmaniasis. editor. Global health observatory data repository. 2016. Available from: https://apps.who.int/gho/data/node.main.NTDLEISH?lang=en
   Google Scholar
• Instituto Ramon y Cajal de Investigacion Sanitaria, World Health Organization. 2019. WHO collaborating centre for clinical management of leishmaniasis (spa-55). (Ed.^(Eds).
   Google Scholar
• World Health Organization W. 2015. Investing to overcome the global impact of neglected tropical diseases. (Ed.^(Eds).
   Google Scholar
• Valero NNH, Uriarte M. Environmental and socioeconomic risk factors associated with visceral and cutaneous leishmaniasis: a systematic review. Parasitol Res. 2020;119(2):365–384.
   PubMed Web of Science ®Google Scholar
• Gadisa E, Tsegaw T, Abera A, et al. Eco-epidemiology of visceral leishmaniasis in Ethiopia. Parasit Vectors. 2015;8(1). DOI:https://doi.org/10.1186/s13071-015-0987-y.
   Google Scholar
• Ngere I, Gufu Boru W, Isack A, et al. Burden and risk factors of cutaneous leishmaniasis in a peri-urban settlement in Kenya, 2016. PLoS ONE. 2020;15(1):e0227697. doi: https://doi.org/10.1371/journal.pone.0227697
   Google Scholar
• Yadon ZE, Rodrigues LC, Davies CR, et al. Indoor and peridomestic transmission of American Cutaneous Leishmaniasis in Northwestern Argentina: a retrospective case-control study. Am J Trop Med Hyg. 2003;68(5):519–526.
   PubMed Web of Science ®Google Scholar
• Hotez PJ, Remme JHF, Buss P, et al. Combating tropical infectious diseases: report of the disease control priorities in developing countries project. Clinl Infect Dis. 2004;38(6):871–878.
   PubMed Web of Science ®Google Scholar
• McIlwee BE, Weis SE, Hosler GA. Incidence of endemic human cutaneous Leishmaniasis in the United States. JAMA Dermatol. 2018;154(9):1032.
   PubMed Web of Science ®Google Scholar
• Garrido-Jareño M, Sahuquillo-Torralba A, Chouman-Arcas R, et al. Cutaneous and mucocutaneous leishmaniasis: experience of a Mediterranean hospital. Parasit Vectors. 2020;13(1). DOI:https://doi.org/10.1186/s13071-020-3901-1.
   Google Scholar
• Clarke CF, Bradley KK, Wright JH, et al. Emergence of Autochthonous Cutaneous Leishmaniasis in Northeastern texas and Southeastern Oklahoma. Am J Trop Med Hyg. 2013;88(1):157–161.
   PubMed Web of Science ®Google Scholar
• Curtin JM, Aronson NE. Leishmaniasis in the United States: emerging Issues in a Region of Low Endemicity. Microorganisms. 2021;9(3):578.
   PubMed Web of Science ®Google Scholar
• de Almeida M, Zheng Y, Nascimento FS, et al. Cutaneous Leishmaniasis caused by an unknown leishmania Strain, Arizona, USA. Emerg Infect Dis. 2021;27(6):1714–1717.
   PubMed Web of Science ®Google Scholar
• Bi K, Chen Y, Zhao S, et al. Current Visceral Leishmaniasis Research: a research review to inspire future study. Biomed Res Int. 2018;2018.
   Web of Science ®Google Scholar
• Hirve S, Kroeger A, Matlashewski G, et al. Towards elimination of visceral leishmaniasis in the Indian subcontinent—Translating research to practice to public health. PLoS Negl Trop Dis. 2017;11(10):e0005889.
   PubMed Web of Science ®Google Scholar
• World Health Organization. 2018. Leishmaniasis. (Ed.^(Eds)
   Google Scholar
• Center for Disease Control and Prevention. 2013. Leishmaniasis. (Ed.^(Eds).
   Google Scholar
• Okwor I, Social UJ. Economic burden of human Leishmaniasis. Am J Trop Med Hyg. 2016;94(3):489–493.
   PubMed Web of Science ®Google Scholar
• Kealey A, Smith R. Neglected tropical diseases: infection, modeling, and control. J Health Care Poor Underserved. 2010;21(1):53–69.
   PubMed Web of Science ®Google Scholar
• Hotez PJ,Ten failings in global neglected tropical diseases control. PLoS Negl Trop Dis. 2017;11(12):e0005896.
   PubMed Web of Science ®Google Scholar
• Brindha J,Balamurali M. M,and Kaushik Chanda. An overview on the therapeutics of neglected infectious diseases-Leishmaniasis and Chagas diseases. Front Chem. 2021;9:622286.
   PubMed Web of Science ®Google Scholar
• World Health Organization W. 2021. Neglected tropical diseases: treating more than one billion people for the fifth consecutive year. (Ed.^(Eds).
   Google Scholar
• World Health Organization. 2020. Ending the neglect to attain the sustainable development goals. A road map for neglected tropical diseases 2021–2030. (Ed.^(Eds).
   Google Scholar
• Ejov M, Dagne D. Strategic framework for leishmaniasis control in the WHO European Region 2014‒2020. (Ed.^(Eds) (2014)
   Google Scholar
• Pan American Health Organization, World Health Organization. Plan of action to strengthen the surveillance and control of leishmaniasis in the Americas. (Ed.^(Eds) (2017)
   Google Scholar
• Volpedo G, Costa L, Ryan N, et al. Nanoparticulate drug delivery systems for the treatment of neglected tropical protozoan diseases. J Venom Anim Toxins Incl Trop Dis. 2019;25:e144118.
   PubMed Web of Science ®Google Scholar
• Berry I, Berrang-Ford L. Leishmaniasis, conflict, and political terror: a spatio-temporal analysis. Soc Sci Med. 2016;167:140–149.
   PubMed Web of Science ®Google Scholar
• Pan American Health Organization Leishmaniasis P. (Ed.^(Eds)
   Google Scholar
• Pavli A, Maltezou HC. Leishmaniasis, an emerging infection in travelers. Int J Infect Dis. 2010;14(12):e1032–1039.
   PubMed Web of Science ®Google Scholar
• Hamer DH, Rizwan A, Freedman DO, et al. GeoSentinel: past, present and future†. J Travel Med. 2020;27(8). DOI:https://doi.org/10.1093/jtm/taaa219
   Google Scholar
• Koch LK, Kochmann J, Klimpel S, et al. Modeling the climatic suitability of leishmaniasis vector species in Europe. Sci Rep. 2017;7(1):13325.
   PubMed Web of Science ®Google Scholar
• Purse BV, Masante D, Golding N, et al. How will climate change pathways and mitigation options alter incidence of vector-borne diseases? A framework for leishmaniasis in South and Meso-America. PLoS One. 2017;12(10):e0183583.
   PubMed Web of Science ®Google Scholar
• Charrahy Z, Yaghoobi-Ershadi MR, Shirzadi MR, et al. Climate change and its effect on the vulnerability to zoonotic cutaneous leishmaniasis in Iran. Transbound Emerg Dis. 2021. DOI:https://doi.org/10.1111/tbed.14115.
   Google Scholar
• Ready PD. Leishmaniasis emergence and climate change. Rev Sci Tech. 2008;27(2):399–412.
   PubMed Web of Science ®Google Scholar
• González C, Wang O, Strutz SE, et al. Climate change and risk of leishmaniasis in north america: predictions from ecological niche models of vector and reservoir species. PLoS Negl Trop Dis. 2010;4(1):e585.
   PubMed Web of Science ®Google Scholar
• Millán J, Ferroglio E, Solano-Gallego L. Role of wildlife in the epidemiology of Leishmania infantum infection in Europe. Parasitol Res. 2014;113(6):2005–2014.
   PubMed Web of Science ®Google Scholar
• Harhay MO, Olliaro PL, Costa DL, et al. Urban parasitology: visceral leishmaniasis in Brazil. Trends Parasitol. 2011;27(9):403–409.
   PubMed Web of Science ®Google Scholar
• Moreno J. Assessment of vaccine-induced immunity against Canine Visceral Leishmaniasis. Front Vet Sci. 2019;6:168.
   PubMed Web of Science ®Google Scholar
• Sousa-Paula LC, Silva LGD, Sales KGDS, et al. Failure of the dog culling strategy in controlling human visceral leishmaniasis in Brazil: a screening coverage issue? PLoS Negl Trop Dis. 2019;13(6):e0007553.
   PubMed Web of Science ®Google Scholar
• Dantas-Torres F, Miró G, Bowman DD, et al. Culling dogs for Zoonotic Visceral Leishmaniasis control: the wind of change. Trends Parasitol. 2019;35(2):97–101.
   PubMed Web of Science ®Google Scholar
• Ribeiro RR, Michalick MSM, Da Silva ME, et al. Canine Leishmaniasis: an overview of the current status and strategies for control. Biomed Res Int. 2018;2018:3296893.
   PubMed Web of Science ®Google Scholar
• Wagner V, Douanne N, Fernandez-Prada C. Leishmania infantum infection in a dog imported from Morocco. Can Vet J. 2020;61(9):963–965.
   PubMed Web of Science ®Google Scholar
• Velez R, Gállego M. Commercially approved vaccines for canine leishmaniosis: a review of available data on their safety and efficacy. Trop Med Int Health. 2020;25(5):540–557.
   PubMed Web of Science ®Google Scholar
• Zhang WW, Karmakar S, Gannavaram S, et al. A second generation leishmanization vaccine with a markerless attenuated Leishmania major strain using CRISPR gene editing. Nat Commun. 2020;11(1):3461.
   PubMed Web of Science ®Google Scholar
• Mendonça SC. Differences in immune responses against Leishmania induced by infection and by immunization with killed parasite antigen: implications for vaccine discovery. Parasit Vectors. 2016;9(1):492.
   PubMed Web of Science ®Google Scholar
• Saljoughian N, Taheri T, Rafati S. Live vaccination tactics: possible approaches for controlling visceral leishmaniasis. Front Immunol. 2014;5:134.
   PubMed Web of Science ®Google Scholar
• Le Rutte EA, Coffeng LE, Malvolti S, et al. The potential impact of human visceral leishmaniasis vaccines on population incidence. PLoS Negl Trop Dis. 2020;14(7):e0008468.
   PubMed Web of Science ®Google Scholar
• Michel G, Pomares C, Ferrua B, et al. Importance of worldwide asymptomatic carriers of Leishmania infantum (L. chagasi) in human. Acta Trop. 2011;119(2–3):69–75.
   PubMed Web of Science ®Google Scholar
• Molina R, Ghosh D, Carrillo E, et al. Infectivity of Post-Kala-azar Dermal Leishmaniasis patients to sand flies: revisiting a proof of concept in the context of the Kala-azar elimination program in the Indian subcontinent. Clin Infect Dis. 2017;65(1):150–153.
   PubMed Web of Science ®Google Scholar
• Asfaram S, Fakhar M, Mohebali M, et al. Asymptomatic human blood donors carriers of Leishmania infantum: potential reservoirs for visceral leishmaniasis in northwestern Iran. Transfus Apher Sci. 2017;56(3):474–479.
   PubMed Web of Science ®Google Scholar
• Singh OP, Tiwary P, Kushwaha AK, et al. Xenodiagnosis to evaluate the infectiousness of humans to sandflies in an area endemic for visceral leishmaniasis in Bihar, India: a transmission-dynamics study. Lancet Microbe. 2021;2(1):e23–e31.
   PubMedGoogle Scholar
• Bacon KM, Hotez PJ, Kruchten SD, et al. The potential economic value of a cutaneous leishmaniasis vaccine in seven endemic countries in the Americas. Vaccine. 2013;31(3):480–486.
   PubMed Web of Science ®Google Scholar
• Lee BY, Bacon KM, Shah M, et al. The economic value of a visceral leishmaniasis vaccine in Bihar state, India. Am J Trop Med Hyg. 2012;86(3):417–425.
   PubMed Web of Science ®Google Scholar
• Cecílio P, Oristian J, Meneses C, et al. Engineering a vector-based pan-Leishmania vaccine for humans: proof of principle. Sci Rep. 2020;10(1):18653.
   PubMed Web of Science ®Google Scholar
• Srivastava S, Shankar P, Mishra J, et al. Possibilities and challenges for developing a successful vaccine for leishmaniasis. Parasit Vectors. 2016;9(1):277.
   PubMed Web of Science ®Google Scholar
• Modabber F. Vaccines against leishmaniasis. Ann Trop Med Parasitol. 1995;89(Suppl 1):83–88.
   PubMedGoogle Scholar
• Noazin S, Modabber F, Khamesipour A, et al. First generation leishmaniasis vaccines: a review of field efficacy trials. Vaccine. 2008;26(52):6759–6767.
   PubMed Web of Science ®Google Scholar
• Noazin S, Khamesipour A, Moulton LH, et al. Efficacy of killed whole-parasite vaccines in the prevention of leishmaniasis: a meta-analysis. Vaccine. 2009;27(35):4747–4753.
   PubMed Web of Science ®Google Scholar
• Mayrink W, Williams P, Da Costa CA, et al. An experimental vaccine against American dermal leishmaniasis: experience in the State of Espírito Santo, Brazil. Ann Trop Med Parasitol. 1985;79(3):259–269.
   PubMed Web of Science ®Google Scholar
• Mayrink W, Da Costa CA, Magalhães PA, et al. A field trial of a vaccine against American dermal leishmaniasis. Trans R Soc Trop Med Hyg. 1979;73(4):385–387.
   PubMed Web of Science ®Google Scholar
• Vélez ID, del Pilar Agudelo S, Arbelaez MP, et al. Safety and immunogenicity of a killed Leishmania (L.) amazonensis vaccine against cutaneous leishmaniasis in Colombia: a randomized controlled trial. Trans R Soc Trop Med Hyg. 2000;94(6):698–703.
   PubMed Web of Science ®Google Scholar
• Sharples CE, Shaw MA, Castes M, et al. Immune response in healthy volunteers vaccinated with BCG plus killed leishmanial promastigotes: antibody responses to mycobacterial and leishmanial antigens. Vaccine. 1994;12(15):1402–1412.
   PubMed Web of Science ®Google Scholar
• Armijos RX, Weigel MM, Aviles H, et al. Field trial of a vaccine against New World cutaneous leishmaniasis in an at-risk child population: safety, immunogenicity, and efficacy during the first 12 months of follow-up. J Infect Dis. 1998;177(5):1352–1357.
   PubMed Web of Science ®Google Scholar
• Armijos RX, Weigel MM, Romero L, et al. Field trial of a vaccine against new world cutaneous leishmaniasis in an at-risk child population: how long does protection last? J Infect Dis. 2003;187(12):1959–1961.
   PubMed Web of Science ®Google Scholar
• Armijos RX, Weigel MM, Calvopina M, et al. Safety, immunogenecity, and efficacy of an autoclaved Leishmania amazonensis vaccine plus BCG adjuvant against New World cutaneous leishmaniasis. Vaccine. 2004;22(9–10):1320–1326.
   PubMed Web of Science ®Google Scholar
• Vélez ID, Gilchrist K, Arbelaez MP, et al. Failure of a killed Leishmania amazonensis vaccine against American cutaneous leishmaniasis in Colombia. Trans R Soc Trop Med Hyg. 2005;99(8):593–598.
   PubMed Web of Science ®Google Scholar
• Sharifi I, FeKri AR, Aflatonian MR, et al. Randomised vaccine trial of single dose of killed Leishmania major plus BCG against anthroponotic cutaneous leishmaniasis in Bam, Iran. Lancet. 1998;351(9115):1540–1543.
   PubMed Web of Science ®Google Scholar
• Alimohammadian MH, Khamesipour A, Darabi H, et al. The role of BCG in human immune responses induced by multiple injections of autoclaved Leishmania major as a candidate vaccine against leishmaniasis. Vaccine. 2002;21(3–4):174–180.
   PubMed Web of Science ®Google Scholar
• Bózner P, Gombosová A, Valent M, et al. Proteinases of Trichomonas vaginalis: antibody response in patients with urogenital trichomoniasis. Parasitology. 1992;105(Pt 3):387–391.
   PubMed Web of Science ®Google Scholar
• Khalil EA, El Hassan AM, Zijlstra EE, et al. Autoclaved Leishmania major vaccine for prevention of visceral leishmaniasis: a randomised, double-blind, BCG-controlled trial in Sudan. Lancet. 2000;356(9241):1565–1569.
   PubMed Web of Science ®Google Scholar
• Satti IN, Osman HY, Daifalla NS, et al. Immunogenicity and safety of autoclaved Leishmania major plus BCG vaccine in healthy Sudanese volunteers. Vaccine. 2001;19(15–16):2100–2106.
   PubMed Web of Science ®Google Scholar
• Momeni AZ, Jalayer T, Emamjomeh M, et al. A randomised, double-blind, controlled trial of a killed L. major vaccine plus BCG against zoonotic cutaneous leishmaniasis in Iran. Vaccine. 1999;17(5):466–472.
   PubMed Web of Science ®Google Scholar
• Mahmoodi M, Khamesipour A, Dowlati Y, et al. Immune response measured in human volunteers vaccinated with autoclaved Leishmania major vaccine mixed with low dose of BCG. Clin Exp Immunol. 2003;134(2):303–308.
   PubMed Web of Science ®Google Scholar
• Nagill R, Kaur S. Vaccine candidates for leishmaniasis: a review. Int Immunopharmacol. 2011;11(10):1464–1488.
   PubMed Web of Science ®Google Scholar
• Coutinho De Oliveira B, Duthie MS, Alves PVR. Vaccines for leishmaniasis and the implications of their development for American tegumentary leishmaniasis. Hum Vaccin Immunother. 2020;16(4):919–930.
   PubMed Web of Science ®Google Scholar
• Peacock CS, Seeger K, Harris D, et al. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet. 2007;39(7):839–847.
   PubMed Web of Science ®Google Scholar
• Kumari S, Kumar A, Samant M, et al. Discovery of novel vaccine candidates and drug targets against visceral leishmaniasis using proteomics and transcriptomics. Curr Drug Targets. 2008;9(11):938–947.
   PubMed Web of Science ®Google Scholar
• De Brito RCF, Cardoso JMO, Reis LES, et al. Peptide Vaccines for Leishmaniasis. Front Immunol. 2018;9:1043.
   PubMed Web of Science ®Google Scholar
• Alvar J, Croft SL, Kaye P, et al. Case study for a vaccine against leishmaniasis. Vaccine. 2013;31(Suppl 2):B244–249.
   PubMed Web of Science ®Google Scholar
• Singh B, Sundar S. Leishmaniasis: vaccine candidates and perspectives. Vaccine. 2012;30(26):3834–3842.
   PubMed Web of Science ®Google Scholar
• Gillespie PM, Beaumier CM, Strych U, et al. Status of vaccine research and development of vaccines for leishmaniasis. Vaccine. 2016;34(26):2992–2995.
   PubMed Web of Science ®Google Scholar
• Bertholet S, Goto Y, Carter L, et al. Optimized subunit vaccine protects against experimental leishmaniasis. Vaccine. 2009;27(50):7036–7045.
   PubMed Web of Science ®Google Scholar
• Coler RN, Duthie MS, Hofmeyer KA, et al. From mouse to man: safety, immunogenicity and efficacy of a candidate leishmaniasis vaccine LEISH-F3+GLA-SE. Clin Transl Immunology. 2015;4(4):e35.
   PubMedGoogle Scholar
• Raman VS, Duthie MS, Fox CB, et al. Adjuvants for Leishmania vaccines: from models to clinical application. Front Immunol. 2012;3:144.
   PubMed Web of Science ®Google Scholar
• Askarizadeh A, Jaafari MR, Khamesipour A, et al. Liposomal adjuvant development for leishmaniasis vaccines. Ther Adv Vaccines. 2017;5(4–5):85–101.
   PubMedGoogle Scholar
• Vogel FR, Hem SL. Chapter 5 - Immunologic adjuvants. In: Vaccines. (editor) Elsevier;2008. p. 59–71.
   Google Scholar
• Carvalho EM, Johnson WD, Barreto E, et al. Cell mediated immunity in American cutaneous and mucosal leishmaniasis. J Immunol. 1985;135(6):4144–4148.
   PubMed Web of Science ®Google Scholar
• Rogers ME. The role of leishmania proteophosphoglycans in sand fly transmission and infection of the Mammalian host. Front Microbiol. 2012;3:223.
   PubMed Web of Science ®Google Scholar
• Abdeladhim M, Kamhawi S, Valenzuela JG. What’s behind a sand fly bite? The profound effect of sand fly saliva on host hemostasis, inflammation and immunity. Infect Genet Evol. 2014;28:691–703.
   PubMed Web of Science ®Google Scholar
• Gomes R, Oliveira F. The immune response to sand fly salivary proteins and its influence on leishmania immunity. Front Immunol. 2012;3:110.
   PubMed Web of Science ®Google Scholar
• Giraud E, Svobodová M, Müller I, et al. Promastigote secretory gel from natural and unnatural sand fly vectors exacerbate. Parasitology. 2019;146(14):1796–1802.
   PubMed Web of Science ®Google Scholar
• Martin-Martin I, Chagas AC, Guimaraes-Costa AB, et al. Immunity to LuloHya and Lundep, the salivary spreading factors from Lutzomyia longipalpis, protects against Leishmania major infection. PLoS Pathog. 2018;14(5):e1007006.
   PubMed Web of Science ®Google Scholar
• Gomes R, Teixeira C, Teixeira MJ, et al. Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Proc Natl Acad Sci U S A. 2008;105(22):7845–7850.
   PubMed Web of Science ®Google Scholar
• Oliveira F, Rowton E, Aslan H, et al. A sand fly salivary protein vaccine shows efficacy against vector-transmitted cutaneous leishmaniasis in nonhuman primates. Sci Transl Med. 2015;7(290):290ra290.
   Web of Science ®Google Scholar
• Tavares NM, Silva RA, Costa DJ, et al. Lutzomyia longipalpis saliva or salivary protein LJM19 protects against Leishmania braziliensis and the saliva of its vector, Lutzomyia intermedia. PLoS Negl Trop Dis. 2011;5(5):e1169.
   PubMed Web of Science ®Google Scholar
• Gomes R, Oliveira F, Teixeira C, et al. Immunity to sand fly salivary protein LJM11 modulates host response to vector-transmitted leishmania conferring ulcer-free protection. J Invest Dermatol. 2012;132(12):2735–2743.
   PubMed Web of Science ®Google Scholar
• Collin N, Gomes R, Teixeira C, et al. Sand fly salivary proteins induce strong cellular immunity in a natural reservoir of visceral leishmaniasis with adverse consequences for Leishmania. PLoS Pathog. 2009;5(5):e1000441.
   PubMed Web of Science ®Google Scholar
• Reed SG, Coler RN, Mondal D, et al. Leishmania vaccine development: exploiting the host-vector-parasite interface. Expert Rev Vaccines. 2016;15(1):81–90.
   PubMed Web of Science ®Google Scholar
• Duthie MS, Van Hoeven N, MacMillen Z, et al. Heterologous immunization with defined RNA and subunit vaccines enhances T cell responses that protect against. Front Immunol. 2018;9(2420). DOI:https://doi.org/10.3389/fimmu.2018.02420.
   Google Scholar
• Liu MA, Wahren B, Karlsson Hedestam GB. DNA vaccines: recent developments and future possibilities. Hum Gene Ther. 2006;17(11):1051–1061.
   PubMed Web of Science ®Google Scholar
• Gurunathan S, Sacks DL, Brown DR, et al. Vaccination with DNA encoding the immunodominant LACK parasite antigen confers protective immunity to mice infected with Leishmania major. J Exp Med. 1997;186(7):1137–1147.
   PubMed Web of Science ®Google Scholar
• Solioz N, Blum-Tirouvanziam U, Jacquet R, et al. The protective capacities of histone H1 against experimental murine cutaneous leishmaniasis. Vaccine. 1999;18(9–10):850–859.
   PubMed Web of Science ®Google Scholar
• Xu D, Liew FY. Protection against leishmaniasis by injection of DNA encoding a major surface glycoprotein, gp63, of L. major. Immunology. 1995;84(2):173–176.
   PubMed Web of Science ®Google Scholar
• Campos-Neto A, Webb JR, Greeson K, et al. Vaccination with plasmid DNA encoding TSA/LmSTI1 leishmanial fusion proteins confers protection against Leishmania major infection in susceptible BALB/c mice. Infect Immun. 2002;70(6):2828–2836.
   PubMed Web of Science ®Google Scholar
• Aguilar-Be I, da Silva Zardo R, Paraguai de Souza E, et al. Cross-protective efficacy of a prophylactic Leishmania donovani DNA vaccine against visceral and cutaneous murine leishmaniasis. Infect Immun. 2005;73(2):812–819.
   PubMed Web of Science ®Google Scholar
• Sukumaran B, Tewary P, Saxena S, et al. Vaccination with DNA encoding ORFF antigen confers protective immunity in mice infected with Leishmania donovani. Vaccine. 2003;21(11–12):1292–1299.
   PubMed Web of Science ®Google Scholar
• Borja-Cabrera GP, Santos FB, Picillo E, et al. Nucleoside hydrolase DNA vaccine against canine visceral leishmaniasis. Procedia Vaccinol. 2009;1(1):104–109.
   PubMedGoogle Scholar
• Rafati S, Salmanian AH, Taheri T, et al. A protective cocktail vaccine against murine cutaneous leishmaniasis with DNA encoding cysteine proteinases of Leishmania major. Vaccine. 2001;19(25–26):3369–3375.
   PubMed Web of Science ®Google Scholar
• Iborra S, Soto M, Carrión J, et al. Vaccination with a plasmid DNA cocktail encoding the nucleosomal histones of Leishmania confers protection against murine cutaneous leishmaniosis. Vaccine. 2004;22(29–30):3865–3876.
   PubMed Web of Science ®Google Scholar
• Rodríguez-Cortés A, Ojeda A, López-Fuertes L, et al. Vaccination with plasmid DNA encoding KMPII, TRYP, LACK and GP63 does not protect dogs against Leishmania infantum experimental challenge. Vaccine. 2007;25(46):7962–7971.
   PubMed Web of Science ®Google Scholar
• Campbell K, Diao H, Ji J, et al. DNA immunization with the gene encoding P4 nuclease of Leishmania amazonensis protects mice against cutaneous Leishmaniasis. Infect Immun. 2003;71(11):6270–6278.
   PubMed Web of Science ®Google Scholar
• Xu D, McSorley SJ, Chatfield SN, et al. Protection against Leishmania major infection in genetically susceptible BALB/c mice by gp63 delivered orally in attenuated Salmonella typhimurium (AroA- AroD-). Immunology. 1995;85(1):1–7.
   PubMed Web of Science ®Google Scholar
• Walker PS, Scharton-Kersten T, Rowton ED, et al. Genetic immunization with glycoprotein 63 cDNA results in a helper T cell type 1 immune response and protection in a murine model of leishmaniasis. Hum Gene Ther. 1998;9(13):1899–1907.
   PubMed Web of Science ®Google Scholar
• Dumonteil E, Andrade-Narvarez F, Escobedo-Ortegon J, et al. Comparative study of DNA vaccines encoding various antigens against Leishmania mexicana. Dev Biol (Basel). 2000;104:135–141.
   PubMedGoogle Scholar
• Dumonteil E, Maria Jesus RS, Javier EO. Maria del Rosario GM. DNA vaccines induce partial protection against Leishmania mexicana. Vaccine. 2003;21(17–18):2161–2168.
   PubMed Web of Science ®Google Scholar
• López-Fuertes L, Pérez-Jiménez E, Vila-Coro AJ, et al. DNA vaccination with linear minimalistic (MIDGE) vectors confers protection against Leishmania major infection in mice. Vaccine. 2002;21(3–4):247–257.
   PubMed Web of Science ®Google Scholar
• Gomes DC, Pinto EF, de Melo LD, et al. Intranasal delivery of naked DNA encoding the LACK antigen leads to protective immunity against visceral leishmaniasis in mice. Vaccine. 2007;25(12):2168–2172.
   PubMed Web of Science ®Google Scholar
• Marques-da-silva EA, Coelho EA, Gomes DC, et al. Intramuscular immunization with p36(LACK) DNA vaccine induces IFN-gamma production but does not protect BALB/c mice against Leishmania chagasi intravenous challenge. Parasitol Res. 2005;98(1):67–74.
   PubMed Web of Science ®Google Scholar
• Melby PC, Yang J, Zhao W, et al. Leishmania donovanip36(LACK) DNA vaccine is highly immunogenic but not protective against experimental Visceral Leishmaniasis. Infect Immun. 2001;69(8):4719–4725.
   PubMed Web of Science ®Google Scholar
• Kumar A, Samant M. DNA vaccine against visceral leishmaniasis: a promising approach for prevention and control. Parasite Immunol. 2016;38(5):273–281.
   PubMed Web of Science ®Google Scholar
• Gonzalo RM, Del Real G, Rodriguez JR, et al. A heterologous prime-boost regime using DNA and recombinant vaccinia virus expressing the Leishmania infantum P36/LACK antigen protects BALB/c mice from cutaneous leishmaniasis. Vaccine. 2002;20(7–8):1226–1231.
   PubMed Web of Science ®Google Scholar
• Kardani K, Bolhassani A, Shahbazi S. Prime-boost vaccine strategy against viral infections: mechanisms and benefits. Vaccine. 2016;34(4):413–423.
   PubMed Web of Science ®Google Scholar
• Ramiro MJ, Zárate JJ, Hanke T, et al. Protection in dogs against visceral leishmaniasis caused by Leishmania infantum is achieved by immunization with a heterologous prime-boost regime using DNA and vaccinia recombinant vectors expressing LACK. Vaccine. 2003;21(19–20):2474–2484.
   PubMed Web of Science ®Google Scholar
• Xiao-wen H, Shu-han S, Zhen-lin H, et al. Augmented humoral and cellular immune responses of a hepatitis B DNA vaccine encoding HBsAg by protein boosting. Vaccine. 2005;23(14):1649–1656.
   PubMed Web of Science ®Google Scholar
• Cui Z. DNA vaccine. Adv Genet. 2005;54:257–289.
   PubMed Web of Science ®Google Scholar
• Restifo NP, Ying H, Hwang L, et al. The promise of nucleic acid vaccines. Gene Ther. 2000;7(2):89–92.
   PubMed Web of Science ®Google Scholar
• Hobernik D, Bros M, Vaccines-How Far DNA. From Clinical Use? Int J Mol Sci. 2018;19(11):3605. doi: https://doi.org/10.3390/ijms19113605
   Google Scholar
• Pandey SC, Kumar A, Samant M. Genetically modified live attenuated vaccine: a potential strategy to combat visceral leishmaniasis. Parasite Immunol. 2020;42(9):e12732.
   PubMed Web of Science ®Google Scholar
• Zabala-Peñafiel A, Todd D, Daneshvar H, et al. The potential of live attenuated vaccines against Cutaneous Leishmaniasis. Exp Parasitol. 2020;210:107849.
   PubMed Web of Science ®Google Scholar
• Titus RG, Gueiros-Filho FJ, de Freitas LA, et al. Development of a safe live Leishmania vaccine line by gene replacement. Proc Natl Acad Sci U S A. 1995;92(22):10267–10271.
   PubMed Web of Science ®Google Scholar
• Muyombwe A, Olivier M, Harvie P, et al. Protection against Leishmania major challenge infection in mice vaccinated with live recombinant parasites expressing a cytotoxic gene. J Infect Dis. 1998;177(1):188–195.
   PubMed Web of Science ®Google Scholar
• Kumari S, Samant M, Khare P, et al. Photodynamic vaccination of hamsters with inducible suicidal mutants of Leishmania amazonensis elicits immunity against visceral leishmaniasis. Eur J Immunol. 2009;39(1):178–191.
   PubMed Web of Science ®Google Scholar
• Davoudi N, Tate CA, Warburton C, et al. Development of a recombinant Leishmania major strain sensitive to ganciclovir and 5-fluorocytosine for use as a live vaccine challenge in clinical trials. Vaccine. 2005;23(9):1170–1177.
   PubMed Web of Science ®Google Scholar
• Mitchell GF, Handman E, Spithill TW. Vaccination against cutaneous leishmaniasis in mice using nonpathogenic cloned promastigotes of Leishmania major and importance of route of injection. Aust J Exp Biol Med Sci. 1984;62(Pt 2):145–153.
   PubMedGoogle Scholar
• Gorczynski RM. Immunization of susceptible BALB/c mice against Leishmania braziliensis. II. Use of temperature-sensitive avirulent clones of parasite for vaccination purposes. Cell Immunol. 1985;94(1):11–20.
   PubMed Web of Science ®Google Scholar
• Rivier D, Shah R, Bovay P, et al. Vaccine development against cutaneous leishmaniasis. Subcutaneous administration of radioattenuated parasites protects CBA mice against virulent Leishmania major challenge. Parasite Immunol. 1993;15(2):75–84.
   PubMed Web of Science ®Google Scholar
• Kimsey PB, Theodos CM, Mitchen TK, et al. An avirulent lipophosphoglycan-deficient Leishmania major clone induces CD4+ T cells which protect susceptible BALB/c mice against infection with virulent L. major. Infect Immun. 1993;61(12):5205–5213.
   PubMed Web of Science ®Google Scholar
• Daneshvar H, Coombs GH, Hagan P, et al. Leishmania mexicana and Leishmania major: attenuation of wild-type parasites and vaccination with the attenuated lines. J Infect Dis. 2003;187(10):1662–1668.
   PubMed Web of Science ®Google Scholar
• Papadopoulou B, Roy G, Breton M, et al. Reduced infectivity of a Leishmania donovani biopterin transporter genetic mutant and its use as an attenuated strain for vaccination. Infect Immun. 2002;70(1):62–68.
   PubMed Web of Science ®Google Scholar
• Dey R, Meneses C, Salotra P, et al. Characterization of a Leishmania stage-specific mitochondrial membrane protein that enhances the activity of cytochrome c oxidase and its role in virulence. Mol Microbiol. 2010;77(2):399–414.
   PubMed Web of Science ®Google Scholar
• Dey R, Dagur PK, Selvapandiyan A, et al. Live attenuated Leishmania donovani p27 gene knockout parasites are nonpathogenic and elicit long-term protective immunity in BALB/c mice. J Immunol. 2013;190(5):2138–2149.
   PubMed Web of Science ®Google Scholar
• Carrión J, Folgueira C, Soto M, et al. Leishmania infantum HSP70-II null mutant as candidate vaccine against leishmaniasis: a preliminary evaluation. Parasit Vectors. 2011;4(1):150.
   PubMed Web of Science ®Google Scholar
• Solana JC, Ramírez L, Cook EC, et al. Subcutaneous Immunization of Leishmania HSP70-II null mutant line reduces the severity of the experimental Visceral Leishmaniasis in BALB/c mice. Vaccines (Basel). 2020;8(1).
   PubMed Web of Science ®Google Scholar
• Soto M, Ramírez L, Solana JC, et al. Inoculation of the Leishmania infantum HSP70-II null mutant induces long-Term protection against L. amazonensis Infection in BALB/c mice. Microorganisms. 2021;9(2):363. doi: https://doi.org/10.3390/microorganisms9020363.
   Google Scholar
• Solana JC, Ramírez L, Corvo L, et al. Vaccination with a Leishmania infantum HSP70-II null mutant confers long-term protective immunity against Leishmania major infection in two mice models. PLoS Negl Trop Dis. 2017;11(5):e0005644.
   PubMed Web of Science ®Google Scholar
• Santi AMM, Lanza JS, Tunes LG, et al. Growth arrested live-attenuated Leishmania infantum KHARON1 null mutants display cytokinesis defect and protective immunity in mice. Sci Rep. 2018;8(1):11627.
   PubMed Web of Science ®Google Scholar
• Selvapandiyan A, Dey R, Nylen S, et al. Intracellular replication-deficient Leishmania donovani induces long lasting protective immunity against visceral leishmaniasis. J Immunol. 2009;183(3):1813–1820.
   PubMed Web of Science ®Google Scholar
• Karmakar S, Ismail N, Oliveira F, et al. Preclinical validation of a live attenuated dermotropic Leishmania vaccine against vector transmitted fatal visceral leishmaniasis. Commun Biol. 2021;4(1):1–14.
   PubMed Web of Science ®Google Scholar
• Zijlstra EE, el-Hassan AM, Ismael A, et al. Endemic kala-azar in eastern Sudan: a longitudinal study on the incidence of clinical and subclinical infection and post-kala-azar dermal leishmaniasis. Am J Trop Med Hyg. 994;51(6):826–836.
   Google Scholar
• Bern C, Amann J, Haque R, et al. Loss of leishmanin skin test antigen sensitivity and potency in a longitudinal study of visceral leishmaniasis in Bangladesh. Am J Trop Med Hyg. 2006;75(4):744–748.
   PubMed Web of Science ®Google Scholar
• Montenegro J. 1926. A cutis-reação na leishmaniose. Anais da Faculdade de Medicina de São Paulo. 1:323–330.
   Google Scholar
• Burza S, Croft SL, Boelaert M. Leishmaniasis. Lancet. 2018;392(10151):951–970.
   PubMed Web of Science ®Google Scholar
• Poulter LW, Seymour GJ, Duke O, et al. Immunohistological analysis of delayed-type hypersensitivity in man. Cell Immunol. 1982;74(2):358–369.
   PubMed Web of Science ®Google Scholar
• Cher DJ, Mosmann TR. Two types of murine helper T cell clone. II. Delayed-type hypersensitivity is mediated by TH1 clones. J Immunol. 1987;138(11):3688–3694.
   PubMed Web of Science ®Google Scholar
• Pacheco-Fernandez T, Volpedo G, Gannavaram S, et al. Revival of Leishmanization and Leishmanin. Front Cell Infect Microbiol. 2021;11:639801.
   PubMed Web of Science ®Google Scholar
• Mohebali M, Nadim A, Khamesipour A. An overview of leishmanization experience: a successful control measure and a tool to evaluate candidate vaccines. Acta Trop. 2019;200:105173.
   PubMed Web of Science ®Google Scholar
• Nadim A, Javadian E, Tahvildar-Bidruni G, et al. Effectiveness of leishmanization in the control of cutaneous leishmaniasis. Bull Soc Pathol Exot Filiales. 1983;76(4):377–383.
   PubMed Web of Science ®Google Scholar
• Nadim AJ, Mohebali E. The experience of leishmanization in the Islamic Republic of Iran. East Mediterr Health J. 1997;3(2): 284–289. M.
   Google Scholar
• Fatemi M, Yaghoobi-Ershadi MR, Mohebali M, et al. The potential role of humans in the transmission cycle of leishmania major (Kinetoplastida: trypanosomatidae), the causative agent of the old World Zoonotic Cutaneous Leishmaniasis. J Med Entomol. 2018;55(6):1588–1593.
   PubMed Web of Science ®Google Scholar
• Denise H, Coombs GH, Mottram JC. Generation of Leishmania mutants lacking antibiotic resistance genes using a versatile hit-and-run targeting strategy. FEMS Microbiol Lett. 2004;235(1):89–94.
   PubMed Web of Science ®Google Scholar
• Seyed N, Peters NC, Rafati S. Translating observations from leishmanization into Non-Living Vaccines: the potential of dendritic cell-based vaccination strategies against. Front Immunol. 2018;9:1227.
   PubMed Web of Science ®Google Scholar
• Lestinova T, Rohousova I, Sima M, et al. Insights into the sand fly saliva: blood-feeding and immune interactions between sand flies, hosts, and Leishmania. PLoS Negl Trop Dis. 2017;11(7):e0005600.
   PubMed Web of Science ®Google Scholar
• Peters NC, Kimblin N, Secundino N, et al. Vector transmission of leishmania abrogates vaccine-induced protective immunity. PLoS Pathog. 2009;5(6):e1000484.
   PubMed Web of Science ®Google Scholar
• Peters NC, Bertholet S, Lawyer PG, et al. Evaluation of recombinant Leishmania polyprotein plus glucopyranosyl lipid A stable emulsion vaccines against sand fly-transmitted Leishmania major in C57BL/6 mice. J Immunol. 2012;189(10):4832–4841.
   PubMed Web of Science ®Google Scholar
• Stamper LW, Patrick RL, Fay MP, et al. Infection parameters in the sand fly vector that predict transmission of Leishmania major. PLoS Negl Trop Dis. 2011;5(8):e1288.
   PubMed Web of Science ®Google Scholar
• Halioua C. 2018OWJC: Why are drugs more profitable than vaccines? (Health economics working paper). (Ed.^(Eds) (Medium).
   Google Scholar
• Dey R, Natarajan G, Bhattacharya P, et al. Characterization of cross-protection by genetically modified live-attenuated Leishmania donovani parasites against Leishmania mexicana. J Immunol. 2014;193(7):3513–3527.
   PubMed Web of Science ®Google Scholar
• Cooper MM, Loiseau C, McCarthy JS, et al. Human challenge models: tools to accelerate the development of malaria vaccines. Expert Rev Vaccines. 2019;18(3):241–251.
   PubMed Web of Science ®Google Scholar
• Ives A, Ronet C, Prevel F, et al. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science. 2011;331(6018):775–778.
   PubMed Web of Science ®Google Scholar