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Published in: Seminars in Immunopathology 3/2020

01-06-2020 | Leishmania | Review

Leishmaniasis immunopathology—impact on design and use of vaccines, diagnostics and drugs

Authors: Paul M. Kaye, Israel Cruz, Albert Picado, Katrien Van Bocxlaer, Simon L. Croft

Published in: Seminars in Immunopathology | Issue 3/2020

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Abstract

Leishmaniasis is a disease complex caused by 20 species of protozoan parasites belonging to the genus Leishmania. In humans, it has two main clinical forms, visceral leishmaniasis (VL) and cutaneous or tegumentary leishmaniasis (CL), as well as several other cutaneous manifestations in a minority of cases. In the mammalian host Leishmania parasites infect different populations of macrophages where they multiply and survive in the phagolysosomal compartment. The progression of both VL and CL depends on the maintenance of a parasite-specific immunosuppressive state based around this host macrophage infection. The complexity and variation of immune responses and immunopathology in humans and the different host interactions of the different Leishmania species has an impact upon the effectiveness of vaccines, diagnostics and drugs.
Literature
1.
go back to reference Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7(5):e35671CrossRef Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7(5):e35671CrossRef
4.
go back to reference Sacks DL (1989) Metacyclogenesis in Leishmania promastigotes. Exp Parasitol 69(1):100–103CrossRef Sacks DL (1989) Metacyclogenesis in Leishmania promastigotes. Exp Parasitol 69(1):100–103CrossRef
10.
go back to reference Rogers ME, Chance ML, Bates PA (2002) The role of promastigote secretory gel in the origin and transmission of the infective stage of Leishmania mexicana by the sandfly Lutzomyia longipalpis. Parasitology 124:495–507CrossRef Rogers ME, Chance ML, Bates PA (2002) The role of promastigote secretory gel in the origin and transmission of the infective stage of Leishmania mexicana by the sandfly Lutzomyia longipalpis. Parasitology 124:495–507CrossRef
11.
15.
go back to reference Kaye P, Scott P (2011) Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol 9(8):604–615CrossRef Kaye P, Scott P (2011) Leishmaniasis: complexity at the host-pathogen interface. Nat Rev Microbiol 9(8):604–615CrossRef
19.
go back to reference Biedermann T, Zimmermann S, Himmelrich H, Gumy A, Egeter O, Sakrauski AK, Seegmuller I, Voigt H, Launois P, Levine AD, Wagner H, Heeg K, Louis JA, Rocken M (2001) IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nat Immunol 2(11):1054–1060. https://doi.org/10.1038/ni725 CrossRefPubMed Biedermann T, Zimmermann S, Himmelrich H, Gumy A, Egeter O, Sakrauski AK, Seegmuller I, Voigt H, Launois P, Levine AD, Wagner H, Heeg K, Louis JA, Rocken M (2001) IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nat Immunol 2(11):1054–1060. https://​doi.​org/​10.​1038/​ni725 CrossRefPubMed
23.
go back to reference Sernee MF, Ralton JE, Nero TL, Sobala LF, Kloehn J, Vieira-Lara MA, Cobbold SA, Stanton L, Pires DEV, Hanssen E, Males A, Ward T, Bastidas LM, van der Peet PL, Parker MW, Ascher DB, Williams SJ, Davies GJ, McConville MJ (2019) A family of dual-activity glycosyltransferase-phosphorylases mediates Mannogen turnover and virulence in Leishmania parasites. Cell Host Microbe 26(3):385–399.e389. https://doi.org/10.1016/j.chom.2019.08.009 CrossRefPubMed Sernee MF, Ralton JE, Nero TL, Sobala LF, Kloehn J, Vieira-Lara MA, Cobbold SA, Stanton L, Pires DEV, Hanssen E, Males A, Ward T, Bastidas LM, van der Peet PL, Parker MW, Ascher DB, Williams SJ, Davies GJ, McConville MJ (2019) A family of dual-activity glycosyltransferase-phosphorylases mediates Mannogen turnover and virulence in Leishmania parasites. Cell Host Microbe 26(3):385–399.e389. https://​doi.​org/​10.​1016/​j.​chom.​2019.​08.​009 CrossRefPubMed
37.
go back to reference Yazici P, Yeniay L, Aydin U, Tasbakan M, Ozutemiz O, Yilmaz R (2008) Visceral leishmaniasis as a rare cause of granulomatosis hepatitis: a case report. Turkiye parazitolojii dergisi 32(1):12–15PubMed Yazici P, Yeniay L, Aydin U, Tasbakan M, Ozutemiz O, Yilmaz R (2008) Visceral leishmaniasis as a rare cause of granulomatosis hepatitis: a case report. Turkiye parazitolojii dergisi 32(1):12–15PubMed
38.
go back to reference Boussoffara T, Boubaker MS, Ben Ahmed M, Mokni M, Guizani I, Ben Salah A, Louzir H (2019) Histological and immunological differences between zoonotic cutaneous leishmaniasis due to Leishmania major and sporadic cutaneous leishmaniasis due to Leishmania infantum. Parasite (Paris, France) 26:9. https://doi.org/10.1051/parasite/2019007 CrossRef Boussoffara T, Boubaker MS, Ben Ahmed M, Mokni M, Guizani I, Ben Salah A, Louzir H (2019) Histological and immunological differences between zoonotic cutaneous leishmaniasis due to Leishmania major and sporadic cutaneous leishmaniasis due to Leishmania infantum. Parasite (Paris, France) 26:9. https://​doi.​org/​10.​1051/​parasite/​2019007 CrossRef
39.
go back to reference Sandoval Pacheco CM, Araujo Flores GV, Favero Ferreira A, Sosa Ochoa W, Ribeiro da Matta VL, Zuniga Valeriano C, Pereira Corbett CE, Dalastra Laurenti M (2018) Histopathological features of skin lesions in patients affected by non-ulcerated or atypical cutaneous leishmaniasis in Honduras, Central America. Int J Exp Pathol 99(5):249–257. https://doi.org/10.1111/iep.12295 CrossRefPubMedPubMedCentral Sandoval Pacheco CM, Araujo Flores GV, Favero Ferreira A, Sosa Ochoa W, Ribeiro da Matta VL, Zuniga Valeriano C, Pereira Corbett CE, Dalastra Laurenti M (2018) Histopathological features of skin lesions in patients affected by non-ulcerated or atypical cutaneous leishmaniasis in Honduras, Central America. Int J Exp Pathol 99(5):249–257. https://​doi.​org/​10.​1111/​iep.​12295 CrossRefPubMedPubMedCentral
53.
go back to reference Ives A, Ronet C, Prevel F, Ruzzante G, Fuertes-Marraco S, Schutz F, Zangger H, Revaz-Breton M, Lye LF, Hickerson SM, Beverley SM, Acha-Orbea H, Launois P, Fasel N, Masina S (2011) Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science (New York, NY) 331(6018):775–778. https://doi.org/10.1126/science.1199326 CrossRef Ives A, Ronet C, Prevel F, Ruzzante G, Fuertes-Marraco S, Schutz F, Zangger H, Revaz-Breton M, Lye LF, Hickerson SM, Beverley SM, Acha-Orbea H, Launois P, Fasel N, Masina S (2011) Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science (New York, NY) 331(6018):775–778. https://​doi.​org/​10.​1126/​science.​1199326 CrossRef
59.
go back to reference Majumder S, Bhattacharjee A, Paul Chowdhury B, Bhattacharyya Majumdar S, Majumdar S (2014) Antigen-pulsed CpG-ODN-activated dendritic cells induce host-protective immune response by regulating the T regulatory cell functioning in Leishmania donovani-infected mice: critical role of CXCL10. Front Immunol 5(261). https://doi.org/10.3389/fimmu.2014.00261 Majumder S, Bhattacharjee A, Paul Chowdhury B, Bhattacharyya Majumdar S, Majumdar S (2014) Antigen-pulsed CpG-ODN-activated dendritic cells induce host-protective immune response by regulating the T regulatory cell functioning in Leishmania donovani-infected mice: critical role of CXCL10. Front Immunol 5(261). https://​doi.​org/​10.​3389/​fimmu.​2014.​00261
61.
go back to reference Das S, Freier A, Boussoffara T, Das S, Oswald D, Losch FO, Selka M, Sacerdoti-Sierra N, Schonian G, Wiesmuller KH, Seifert K, Schroff M, Juhls C, Jaffe CL, Roy S, Das P, Louzir H, Croft SL, Modabber F, Walden P (2014) Modular multiantigen T cell epitope-enriched DNA vaccine against human leishmaniasis. Sci Transl Med 6(234):234ra256. https://doi.org/10.1126/scitranslmed.3008222 CrossRef Das S, Freier A, Boussoffara T, Das S, Oswald D, Losch FO, Selka M, Sacerdoti-Sierra N, Schonian G, Wiesmuller KH, Seifert K, Schroff M, Juhls C, Jaffe CL, Roy S, Das P, Louzir H, Croft SL, Modabber F, Walden P (2014) Modular multiantigen T cell epitope-enriched DNA vaccine against human leishmaniasis. Sci Transl Med 6(234):234ra256. https://​doi.​org/​10.​1126/​scitranslmed.​3008222 CrossRef
65.
go back to reference Toepp A, Larson M, Wilson G, Grinnage-Pulley T, Bennett C, Leal-Lima A, Anderson B, Parrish M, Anderson M, Fowler H, Hinman J, Kontowicz E, Jefferies J, Beeman M, Buch J, Saucier J, Tyrrell P, Gharpure R, Cotter C, Petersen C (2018) Randomized, controlled, double-blinded field trial to assess Leishmania vaccine effectiveness as immunotherapy for canine leishmaniosis. Vaccine 36(43):6433–6441. https://doi.org/10.1016/j.vaccine.2018.08.087 CrossRefPubMed Toepp A, Larson M, Wilson G, Grinnage-Pulley T, Bennett C, Leal-Lima A, Anderson B, Parrish M, Anderson M, Fowler H, Hinman J, Kontowicz E, Jefferies J, Beeman M, Buch J, Saucier J, Tyrrell P, Gharpure R, Cotter C, Petersen C (2018) Randomized, controlled, double-blinded field trial to assess Leishmania vaccine effectiveness as immunotherapy for canine leishmaniosis. Vaccine 36(43):6433–6441. https://​doi.​org/​10.​1016/​j.​vaccine.​2018.​08.​087 CrossRefPubMed
66.
go back to reference WHO (2016) Leishmaniasis in high-burden countries: An epidemiological update based on data reported in 2014 WHO Weekly epidemiological record 22 (91):285–296 WHO (2016) Leishmaniasis in high-burden countries: An epidemiological update based on data reported in 2014 WHO Weekly epidemiological record 22 (91):285–296
67.
go back to reference Organization WECotCotLWH (2010) Control of the leishmaniases: report of a meeting of the WHO expert committee on the control of Leishmaniases vol 949. World Health Organization, Geneva Organization WECotCotLWH (2010) Control of the leishmaniases: report of a meeting of the WHO expert committee on the control of Leishmaniases vol 949. World Health Organization, Geneva
68.
go back to reference Ghose AC, Haldar JP, Pal SC, Mishra BP, Mishra KK (1980) Serological investigations on Indian kala-azar. Clin Exp Immunol 40(2):318–326PubMedPubMedCentral Ghose AC, Haldar JP, Pal SC, Mishra BP, Mishra KK (1980) Serological investigations on Indian kala-azar. Clin Exp Immunol 40(2):318–326PubMedPubMedCentral
70.
go back to reference Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, Alvar J, Boelaert M (2007) Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol 5(11):873–882CrossRef Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, Alvar J, Boelaert M (2007) Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol 5(11):873–882CrossRef
73.
go back to reference Pattabhi S, Whittle J, Mohamath R, El-Safi S, Moulton GG, Guderian JA, Colombara D, Abdoon AO, Mukhtar MM, Mondal D, Esfandiari J, Kumar S, Chun P, Reed SG, Bhatia A (2010) Design, development and evaluation of rK28-based point-of-care tests for improving rapid diagnosis of visceral leishmaniasis. PLoS Negl Trop Dis 4(9). https://doi.org/10.1371/journal.pntd.0000822 Pattabhi S, Whittle J, Mohamath R, El-Safi S, Moulton GG, Guderian JA, Colombara D, Abdoon AO, Mukhtar MM, Mondal D, Esfandiari J, Kumar S, Chun P, Reed SG, Bhatia A (2010) Design, development and evaluation of rK28-based point-of-care tests for improving rapid diagnosis of visceral leishmaniasis. PLoS Negl Trop Dis 4(9). https://​doi.​org/​10.​1371/​journal.​pntd.​0000822
75.
go back to reference Mukhtar M, Abdoun A, Ahmed AE, Ghalib H, Reed SG, Boelaert M, Menten J, Khair MM, Howard RF (2015) Diagnostic accuracy of rK28-based immunochromatographic rapid diagnostic tests for visceral leishmaniasis: a prospective clinical cohort study in Sudan. Trans R Soc Trop Med Hyg 109(9):594–600. https://doi.org/10.1093/trstmh/trv060 CrossRefPubMed Mukhtar M, Abdoun A, Ahmed AE, Ghalib H, Reed SG, Boelaert M, Menten J, Khair MM, Howard RF (2015) Diagnostic accuracy of rK28-based immunochromatographic rapid diagnostic tests for visceral leishmaniasis: a prospective clinical cohort study in Sudan. Trans R Soc Trop Med Hyg 109(9):594–600. https://​doi.​org/​10.​1093/​trstmh/​trv060 CrossRefPubMed
77.
go back to reference Subramaniam KS, Austin V, Schocker NS, Montoya AL, Anderson MS, Ashmus RA, Mesri M, Al-Salem W, Almeida IC, Michael K, Acosta-Serrano A (2018) Anti-alpha-Gal antibodies detected by novel neoglycoproteins as a diagnostic tool for Old World cutaneous leishmaniasis caused by Leishmania major. Parasitology 145(13):1758–1764. https://doi.org/10.1017/s0031182018000860 CrossRefPubMed Subramaniam KS, Austin V, Schocker NS, Montoya AL, Anderson MS, Ashmus RA, Mesri M, Al-Salem W, Almeida IC, Michael K, Acosta-Serrano A (2018) Anti-alpha-Gal antibodies detected by novel neoglycoproteins as a diagnostic tool for Old World cutaneous leishmaniasis caused by Leishmania major. Parasitology 145(13):1758–1764. https://​doi.​org/​10.​1017/​s003118201800086​0 CrossRefPubMed
81.
82.
go back to reference Marlais T, Bhattacharyya T, Singh OP, Mertens P, Gilleman Q, Thunissen C, Hinckel BCB, Pearson C, Gardner BL, Airs S, de la Roche M, Hayes K, Hafezi H, Falconar AK, Eisa O, Saad A, Khanal B, Bhattarai NR, Rijal S, Boelaert M, El-Safi S, Sundar S, Miles MA (2018) Visceral Leishmaniasis IgG1 rapid monitoring of cure vs. relapse, and potential for diagnosis of post kala-azar dermal Leishmaniasis. Front Cell Infect Microbiol 8:427. https://doi.org/10.3389/fcimb.2018.00427 CrossRefPubMedPubMedCentral Marlais T, Bhattacharyya T, Singh OP, Mertens P, Gilleman Q, Thunissen C, Hinckel BCB, Pearson C, Gardner BL, Airs S, de la Roche M, Hayes K, Hafezi H, Falconar AK, Eisa O, Saad A, Khanal B, Bhattarai NR, Rijal S, Boelaert M, El-Safi S, Sundar S, Miles MA (2018) Visceral Leishmaniasis IgG1 rapid monitoring of cure vs. relapse, and potential for diagnosis of post kala-azar dermal Leishmaniasis. Front Cell Infect Microbiol 8:427. https://​doi.​org/​10.​3389/​fcimb.​2018.​00427 CrossRefPubMedPubMedCentral
83.
go back to reference Mollett G, Bremer Hinckel BC, Bhattacharyya T, Marlais T, Singh OP, Mertens P, Falconar AK, El-Safi S, Sundar S, Miles MA (2019) Detection of immunoglobulin G1 against rK39 improves monitoring of treatment outcomes in visceral Leishmaniasis. Clin Infect Dis 69(7):1130–1135. https://doi.org/10.1093/cid/ciy1062 CrossRefPubMed Mollett G, Bremer Hinckel BC, Bhattacharyya T, Marlais T, Singh OP, Mertens P, Falconar AK, El-Safi S, Sundar S, Miles MA (2019) Detection of immunoglobulin G1 against rK39 improves monitoring of treatment outcomes in visceral Leishmaniasis. Clin Infect Dis 69(7):1130–1135. https://​doi.​org/​10.​1093/​cid/​ciy1062 CrossRefPubMed
90.
go back to reference Ben Salah A, Zaatour A, Gharbi A, Bettaieb J, Ghawar W, Khedher a Clinical evaluation of CL detect TM rapid test for cutaneous leishmaniasis: performance characteristics when compared to smear microscopy at multiple test sites. In: ASTMH, New Orleans, 2014 Ben Salah A, Zaatour A, Gharbi A, Bettaieb J, Ghawar W, Khedher a Clinical evaluation of CL detect TM rapid test for cutaneous leishmaniasis: performance characteristics when compared to smear microscopy at multiple test sites. In: ASTMH, New Orleans, 2014
91.
98.
go back to reference WHO (2017) Integrating neglected tropical diseases into global health and development: fourth WHO report on neglected tropical diseases. World Health Organisation, WHO (2017) Integrating neglected tropical diseases into global health and development: fourth WHO report on neglected tropical diseases. World Health Organisation,
104.
go back to reference Picado A, Cruz I, Sampath R, Ndung'u JM (2019) An antigen detecting rapid diagnostic test (RDT) to accelerate control and elimination of visceral leishmaniasis. 11th European congress on tropical medicine and international health 113. https://doi.org/10.1093/trstmh/trz0 Picado A, Cruz I, Sampath R, Ndung'u JM (2019) An antigen detecting rapid diagnostic test (RDT) to accelerate control and elimination of visceral leishmaniasis. 11th European congress on tropical medicine and international health 113. https://​doi.​org/​10.​1093/​trstmh/​trz0
112.
go back to reference Aronson N, Herwaldt BL, Libman M, Pearson R, Lopez-Velez R, Weina P, Carvalho E, Ephros M, Jeronimo S, Magill A (2017) Diagnosis and treatment of Leishmaniasis: clinical practice guidelines by the Infectious Diseases Society of America (IDSA) and the American Society of Tropical Medicine and Hygiene (ASTMH). Am J Tropical Med Hyg 96(1):24–45. https://doi.org/10.4269/ajtmh.16-84256 CrossRef Aronson N, Herwaldt BL, Libman M, Pearson R, Lopez-Velez R, Weina P, Carvalho E, Ephros M, Jeronimo S, Magill A (2017) Diagnosis and treatment of Leishmaniasis: clinical practice guidelines by the Infectious Diseases Society of America (IDSA) and the American Society of Tropical Medicine and Hygiene (ASTMH). Am J Tropical Med Hyg 96(1):24–45. https://​doi.​org/​10.​4269/​ajtmh.​16-84256 CrossRef
114.
go back to reference González U, Pinart M, Rengifo-Pardo M, Macaya A, Alvar J, Tweed JA (2009) Interventions for American cutaneous and mucocutaneous leishmaniasis. Cochrane database systematic reviews 15 (2 (CD004834)):1-171 González U, Pinart M, Rengifo-Pardo M, Macaya A, Alvar J, Tweed JA (2009) Interventions for American cutaneous and mucocutaneous leishmaniasis. Cochrane database systematic reviews 15 (2 (CD004834)):1-171
117.
118.
go back to reference Van Bocxlaer K, Caridha D, Black C, Vesely B, Leed S, Sciotti RJ, Wijnant GJ, Yardley V, Braillard S, Mowbray CE, Ioset JR, Croft SL (2019) Novel benzoxaborole, nitroimidazole and aminopyrazoles with activity against experimental cutaneous leishmaniasis. Int J Parasitol Drugs Drug Resist. https://doi.org/10.1016/j.ijpddr.2019.02.002 Van Bocxlaer K, Caridha D, Black C, Vesely B, Leed S, Sciotti RJ, Wijnant GJ, Yardley V, Braillard S, Mowbray CE, Ioset JR, Croft SL (2019) Novel benzoxaborole, nitroimidazole and aminopyrazoles with activity against experimental cutaneous leishmaniasis. Int J Parasitol Drugs Drug Resist. https://​doi.​org/​10.​1016/​j.​ijpddr.​2019.​02.​002
119.
go back to reference Caridha D, Vesely B, van Bocxlaer K, Arana B, Mowbray CE, Rafati S, Uliana S, Reguera R, Kreishman-Deitrick M, Sciotti R, Buffet P, Croft SL (2019) Route map for the discovery and pre-clinical development of new drugs and treatments for cutaneous leishmaniasis. Int J Parasitol Drugs Drug Resist. https://doi.org/10.1016/j.ijpddr.2019.06.003 Caridha D, Vesely B, van Bocxlaer K, Arana B, Mowbray CE, Rafati S, Uliana S, Reguera R, Kreishman-Deitrick M, Sciotti R, Buffet P, Croft SL (2019) Route map for the discovery and pre-clinical development of new drugs and treatments for cutaneous leishmaniasis. Int J Parasitol Drugs Drug Resist. https://​doi.​org/​10.​1016/​j.​ijpddr.​2019.​06.​003
124.
go back to reference Mbui J, Olobo J, Omollo R, Solomos A, Kip AE, Kirigi G, Sagaki P, Kimutai R, Were L, Omollo T, Egondi TW, Wasunna M, Alvar J, Dorlo TPC, Alves F (2019) Pharmacokinetics, safety, and efficacy of an Allometric Miltefosine regimen for the treatment of visceral Leishmaniasis in eastern African children: an open-label, phase II clinical trial. Clin Infect Dis 68(9):1530–1538. https://doi.org/10.1093/cid/ciy747 CrossRefPubMed Mbui J, Olobo J, Omollo R, Solomos A, Kip AE, Kirigi G, Sagaki P, Kimutai R, Were L, Omollo T, Egondi TW, Wasunna M, Alvar J, Dorlo TPC, Alves F (2019) Pharmacokinetics, safety, and efficacy of an Allometric Miltefosine regimen for the treatment of visceral Leishmaniasis in eastern African children: an open-label, phase II clinical trial. Clin Infect Dis 68(9):1530–1538. https://​doi.​org/​10.​1093/​cid/​ciy747 CrossRefPubMed
125.
go back to reference Murray HW (2000) Suppression of posttreatment recurrence of experimental visceral Leishmaniasis in T-cell-deficient mice by oral Miltefosine. Antimicrob Agents Chemother 44(11):3235–3236CrossRef Murray HW (2000) Suppression of posttreatment recurrence of experimental visceral Leishmaniasis in T-cell-deficient mice by oral Miltefosine. Antimicrob Agents Chemother 44(11):3235–3236CrossRef
126.
go back to reference Murray HW, Delph-Etienne S (2000) Visceral leishmanicidal activity of hexadecylphosphocholine (miltefosine) in mice deficient in T cells and activated macrophage microbicidal mechanisms. J Infect Dis 181(2):795–799CrossRef Murray HW, Delph-Etienne S (2000) Visceral leishmanicidal activity of hexadecylphosphocholine (miltefosine) in mice deficient in T cells and activated macrophage microbicidal mechanisms. J Infect Dis 181(2):795–799CrossRef
127.
go back to reference Escobar P, Yardley V, Croft SL (2001) Activities of hexadecylphosphocholine (miltefosine), AmBisome, and sodium stibogluconate (Pentostam) against Leishmania donovani in immunodeficient scid mice. (0066–4804 (Print)) Escobar P, Yardley V, Croft SL (2001) Activities of hexadecylphosphocholine (miltefosine), AmBisome, and sodium stibogluconate (Pentostam) against Leishmania donovani in immunodeficient scid mice. (0066–4804 (Print))
128.
go back to reference Dorlo TP, Balasegaram M, Beijnen JH, de Vries PJ (2012) Miltefosine: a review of its pharmacology and therapeutic efficacy in the treatment of leishmaniaisis. J Antimicrob Chemother 67(11):2576–2597CrossRef Dorlo TP, Balasegaram M, Beijnen JH, de Vries PJ (2012) Miltefosine: a review of its pharmacology and therapeutic efficacy in the treatment of leishmaniaisis. J Antimicrob Chemother 67(11):2576–2597CrossRef
130.
go back to reference Murray HW, Berman JD, Davies CR, Saravia NG (2005) Advances in leishmaniasis. Lancet 366(9496):1577CrossRef Murray HW, Berman JD, Davies CR, Saravia NG (2005) Advances in leishmaniasis. Lancet 366(9496):1577CrossRef
133.
go back to reference Musa AM, Khalil EAG, Mahgoub FAE, Elgawi SHH, Modabber F, Elkadaru AEMY, Aboud MH, Noazin S, Ghalib HW, El-Hassan AM Group/Sudan TLR (2008) Immunochemotherapy of persistent post-kala-azar dermal leishmaniasis: a novel approach to treatment. Trans R Soc Trop Med Hyg 102(1):58–63. https://doi.org/10.1016/j.trstmh.2007.08.006 Musa AM, Khalil EAG, Mahgoub FAE, Elgawi SHH, Modabber F, Elkadaru AEMY, Aboud MH, Noazin S, Ghalib HW, El-Hassan AM Group/Sudan TLR (2008) Immunochemotherapy of persistent post-kala-azar dermal leishmaniasis: a novel approach to treatment. Trans R Soc Trop Med Hyg 102(1):58–63. https://​doi.​org/​10.​1016/​j.​trstmh.​2007.​08.​006
135.
go back to reference Adinolfi LE, Bonventre PF, Vander Pas M, Eppstein DA (1985) Synergistic effect of glucantime and a liposome-encapsulated muramyl dipeptide analog in therapy of experimental visceral leishmaniasis. Infect Immun 48(2):409–416CrossRef Adinolfi LE, Bonventre PF, Vander Pas M, Eppstein DA (1985) Synergistic effect of glucantime and a liposome-encapsulated muramyl dipeptide analog in therapy of experimental visceral leishmaniasis. Infect Immun 48(2):409–416CrossRef
137.
go back to reference Badaro R, Nascimento C, Carvalho JS, Badaro F, Russo D, Ho JL, Reed SG, Johnson WD Jr, Jones TC (1994) Granulocyte-macrophage colony-stimulating factor in combination with pentavalent antimony for the treatment of visceral Leishmaniasis. Eur J Clin Microbiol Infect Dis 13(Suppl 2):S23–S28. https://doi.org/10.1007/bf01973598 CrossRefPubMed Badaro R, Nascimento C, Carvalho JS, Badaro F, Russo D, Ho JL, Reed SG, Johnson WD Jr, Jones TC (1994) Granulocyte-macrophage colony-stimulating factor in combination with pentavalent antimony for the treatment of visceral Leishmaniasis. Eur J Clin Microbiol Infect Dis 13(Suppl 2):S23–S28. https://​doi.​org/​10.​1007/​bf01973598 CrossRefPubMed
138.
go back to reference Almeida R, D'Oliveira A Jr, Machado P, Bacellar O, Ko AI, de Jesus AR, Mobashery N, Brito Santos J, Carvalho EM (1999) Randomized, double-blind study of stibogluconate plus human granulocyte macrophage colony-stimulating factor versus stibogluconate alone in the treatment of cutaneous Leishmaniasis. J Infect Dis 180(5):1735–1737. https://doi.org/10.1086/315082 CrossRefPubMed Almeida R, D'Oliveira A Jr, Machado P, Bacellar O, Ko AI, de Jesus AR, Mobashery N, Brito Santos J, Carvalho EM (1999) Randomized, double-blind study of stibogluconate plus human granulocyte macrophage colony-stimulating factor versus stibogluconate alone in the treatment of cutaneous Leishmaniasis. J Infect Dis 180(5):1735–1737. https://​doi.​org/​10.​1086/​315082 CrossRefPubMed
139.
go back to reference Santos JB, de Jesus AR, Machado PR, Magalhaes A, Salgado K, Carvalho EM, Almeida RP (2004) Antimony plus recombinant human granulocyte-macrophage colony-stimulating factor applied topically in low doses enhances healing of cutaneous Leishmaniasis ulcers: a randomized, double-blind, placebo-controlled study. J Infect Dis 190(10):1793–1796. https://doi.org/10.1086/424848 CrossRefPubMed Santos JB, de Jesus AR, Machado PR, Magalhaes A, Salgado K, Carvalho EM, Almeida RP (2004) Antimony plus recombinant human granulocyte-macrophage colony-stimulating factor applied topically in low doses enhances healing of cutaneous Leishmaniasis ulcers: a randomized, double-blind, placebo-controlled study. J Infect Dis 190(10):1793–1796. https://​doi.​org/​10.​1086/​424848 CrossRefPubMed
143.
go back to reference Buates S, Matlashewski G (1999) Treatment of experimental leishmaniasis with the immunomodulators imiquimod and S-28463: efficacy and mode of action. J Infect Dis 179:1485–1494CrossRef Buates S, Matlashewski G (1999) Treatment of experimental leishmaniasis with the immunomodulators imiquimod and S-28463: efficacy and mode of action. J Infect Dis 179:1485–1494CrossRef
144.
go back to reference Arevalo I, Tulliano G, Quispe A, Spaeth G, Matlashewski G, Llanos-Cuentas A, Pollack H (2007) Role of imiquimod and parenteral meglumine antimoniate in the initial treatment of cutaneous leishmaniasis. Clin Infect Dis 44(12):1549–1554CrossRef Arevalo I, Tulliano G, Quispe A, Spaeth G, Matlashewski G, Llanos-Cuentas A, Pollack H (2007) Role of imiquimod and parenteral meglumine antimoniate in the initial treatment of cutaneous leishmaniasis. Clin Infect Dis 44(12):1549–1554CrossRef
145.
go back to reference Miranda-Verastegui C, Llanos-Cuentas A, Arevalo I, Ward BJ, Matlashewski G (2005) Randomized, double-blind clinical trial of topical imiquimod 5% with parenteral meglumine antimoniate in the treatment of cutaneous leishmaniasis in Peru. Clin Infect Dis 40(10):1395–1403CrossRef Miranda-Verastegui C, Llanos-Cuentas A, Arevalo I, Ward BJ, Matlashewski G (2005) Randomized, double-blind clinical trial of topical imiquimod 5% with parenteral meglumine antimoniate in the treatment of cutaneous leishmaniasis in Peru. Clin Infect Dis 40(10):1395–1403CrossRef
146.
go back to reference Firooz A, Khamesipour A, Ghoorchi MH, Nassiri-Kashani M, Eskandari SE, Khatami A, Hooshmand B, Gorouhi F, Rashighi-Firoozabadi M, Dowlati Y (2006) Imiquimod in combination with meglumine antimoniate for cutaneous leishmaniasis. Arch Dermatol 142(12):1575–1579CrossRef Firooz A, Khamesipour A, Ghoorchi MH, Nassiri-Kashani M, Eskandari SE, Khatami A, Hooshmand B, Gorouhi F, Rashighi-Firoozabadi M, Dowlati Y (2006) Imiquimod in combination with meglumine antimoniate for cutaneous leishmaniasis. Arch Dermatol 142(12):1575–1579CrossRef
157.
go back to reference Sakthianandeswaren A, Elso CM, Simpson K, Curtis JM, Kumar B, Speed TP, Handman E, Foote SJ (2005) The wound repair response controls outcome to cutaneous leishmaniasis. Proc Natl Acad Sci U S A 102(43):15551–15556CrossRef Sakthianandeswaren A, Elso CM, Simpson K, Curtis JM, Kumar B, Speed TP, Handman E, Foote SJ (2005) The wound repair response controls outcome to cutaneous leishmaniasis. Proc Natl Acad Sci U S A 102(43):15551–15556CrossRef
160.
go back to reference Wijnant GJ, Van Bocxlaer K, Yardley V, Harris A, Alavijeh M, Silva-Pedrosa R, Antunes S, Mauricio I, Murdan S, Croft SL (2018) Comparative efficacy, toxicity and biodistribution of the liposomal amphotericin B formulations Fungisome((R)) and AmBisome((R)) in murine cutaneous leishmaniasis. Int J Parasitol Drugs Drug Resist 8 (2):223–228. doi:https://doi.org/10.1016/j.ijpddr.2018.04.001 Wijnant GJ, Van Bocxlaer K, Yardley V, Harris A, Alavijeh M, Silva-Pedrosa R, Antunes S, Mauricio I, Murdan S, Croft SL (2018) Comparative efficacy, toxicity and biodistribution of the liposomal amphotericin B formulations Fungisome((R)) and AmBisome((R)) in murine cutaneous leishmaniasis. Int J Parasitol Drugs Drug Resist 8 (2):223–228. doi:https://​doi.​org/​10.​1016/​j.​ijpddr.​2018.​04.​001
Metadata
Title
Leishmaniasis immunopathology—impact on design and use of vaccines, diagnostics and drugs
Authors
Paul M. Kaye
Israel Cruz
Albert Picado
Katrien Van Bocxlaer
Simon L. Croft
Publication date
01-06-2020
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 3/2020
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-020-00788-y

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