Immune responses in kala-azar

Indian Journal of Medical Research

Volumn 123, Issue 3, 2006, Pages 245-266

  Saha, Samiran ^a   Mondal, Smriti ^a   Banerjee, Antara ^a   Ghose, Jayeeta ^a   Bhowmick, Sudipta ^a   Ali, Nahid ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

Author keywords

CD4+ T cell; CD8+ T cell; Cutaneous leishmaniasis; IFN ; IL 10; IL 12; Immune response; Macrophage; Serodiagnosis; Th1 response; Th2 response; Visceral leishmaniasis

Indexed keywords

ANTIINFECTIVE AGENT; ANTILEISHMANIAL AGENT; ANTIMONY; CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 12; INTERLEUKIN 12 ANTIBODY; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; LEISHMANIA VACCINE; PARASITE ANTIGEN; RECOMBINANT INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA;

CELLULAR IMMUNITY; CYTOKINE PRODUCTION; DIAGNOSTIC PROCEDURE; DRUG DESIGN; ENDEMIC DISEASE; HOST PARASITE INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOREGULATION; INDIA; LEISHMANIA DONOVANI; LEISHMANIASIS; MACROPHAGE; NONHUMAN; PARASITE SURVIVAL; PROTEIN SYNTHESIS INHIBITION; REGULATORY T LYMPHOCYTE; REVIEW; SKIN LEISHMANIASIS; SUPERINFECTION; SYMPTOMATOLOGY; TH1 CELL; TH2 CELL; TUBERCULOSIS; VISCERAL LEISHMANIASIS;

ANIMALS; ANTIGENS, PROTOZOAN; ANTIPROTOZOAL AGENTS; CYTOKINES; HUMANS; IMMUNE SYSTEM; LEISHMANIA; LEISHMANIASIS, VISCERAL; MACROPHAGES; MODELS, BIOLOGICAL;

EID: 33745187998     PISSN: 09715916     EISSN: 09715916     Source Type: Journal    
DOI: None     Document Type: Review

References (198)

1. Desjeux P. Leishmaniasis. Nat Rev Microbiol 2004; 2 : 692-3.
2. Renee H, Wang NE, Halpern J. Leishmaniasis. www.emedicine.com/emerg/topic296.htm. Last Updated: September 13, 2005. eMedicine. Accessed on March 26, 2006.
3. Wilson ME, Jeronimo SM, Pearson RD. Immunopathogenesis of infection with the visceralizing Leishmania species. Microb Pathog 2005; 38 :147-60.
4. Stark CG, Wortmann G. Leishmaniasis. www.emedicine.com/med/topic1275.htm. Last Updated: January 6, 2006. eMedicine. Accessed on March 26, 2006.
5. Brahmachari UN. A tretise on Kala-azar. London: John Bale, Sons & Danielsson; 1928 p. 1-3.
6. Desjeux P. Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 2004; 27 : 305-18.
7. Peters W, Killick-kendrick R, editors. The leishmaniasis in biology and medicine. London: Academic Press; 1987.
8. Sacks D, Kamhawi S. Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu Rev Microbiol 2001; 55: 453-83.
9. Unanue ER, Allen PM. The basis for the immunoregulatory role of macrophages and other accessory cells. Science 1987; 236 : 551-7.
10. Alexander J, Russell DG. The interaction of Leishmania species with macrophages. Adv Parasitol 1992; 31 : 175-254.
11. Reiner NE, Ng W, Wilson CB, McMaster WR, Burchett SK. Modulation of in vitro monocyte cytokine responses to Leishmania donovani. Interferon-gamma prevents parasite-induced inhibition of interleukin 1 production and primes monocytes to respond to Leishmania by producing both tumor necrosis factor-alpha and interleukin 1. J Clin Invest 1990; 85 : 1914-24.
12. Bray RS. Immunodiagnosis of leishmaniasis. In: Cohen S, Sadun EH, editors. Immunology of parasite infections. Oxford, United Kingdom: Blackwell Scientific Publications; 1976 p. 65-76.
13. Neogy AB, Nandy A, Ghosh Dastidar B, Chowdhury AB. Antibody kinetics in kala-azar in response to treatment. Ann Trop Med Parasitol 1987; 81 : 727-9.
14. Badaro R, Jones TC, Carvalho EM, Sampaio D, Reed SG, Barral A, et al. New perspectives on a subclinical form of visceral leishmaniasis. Lancet 1986; 1 : 647-8.
15. Desjeux, P. Human leishmaniasis: epidemiology and public health aspects. World Health Stat Q 1992; 45 : 267-75.
16. Kurtzhals JA, Hey AS, Theander TG, Odera E, Christensen CB, Githure JI, et al. Cellular and humoral immune responses in a population from the Baringo District, Kenya, to Leishmania promastigote lipophosphoglycan. Am J Trop Med Hyg 1992; 46 : 480-8.
17. Sacks DL, Lal SL, Shrivastava SN, Blackwell J, Neva FA. An analysis of T cell responsiveness in Indian kala-azar. J Immunol 1987; 138 : 908-13.
18. Behin R, Jacques L. Immune response to Leishmania. Crit Rev Trop Med 1989; 2 :141-88.
19. Montoya Y, Leon C, Talledo M, Nolasco O, Padilla C, Munoz-Najar U, et al. Recombinant antigens for specific and sensitive serodiagnosis of Latin American tegumentary leishmaniasis. Trans R Soc Trop Med Hyg 1997; 91 : 674-6.
20. Valli LC, Passos VM, Dietze R, Callahan HL, Berman JD, Grogl M. Humoral immune responses among mucosal and cutaneous leishmaniasis patients caused by Leishmania braziliensis. J Parasitol 1999; 85 : 1076-83.
21. Brito ME, Mendonca MG, Gomes YM, Jardim ML, Abath FG. Identification of potentially diagnostic Leishmania braziliensis antigens in human cutaneous leishmaniasis by immunoblot analysis. Clin Diagn Lab Immunol 2000; 7: 318-21.
22. Brito ME, Mendonca MG, Gomes YM, Jardim ML, Abath FG. Dynamics of the antibody response in patients with therapeutic or spontaneous cure of American cutaneous leishmaniasis. Trans R Soc Trop Med Hyg 2001; 95 : 203-6.
23. Romero GA, de la Gloria Orge Orge M, de Farias Guerra MV, Paes MG, de Oliveira Macedo V, de Carvalho EM. Antibody response in patients with cutaneous leishmaniasis infected by Leishmania (Viannia) braziliensis or Leishmania (Viannia) guyanensis in Brazil. Acta Trop 2005; 93: 49-56.
24. Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature 1996; 383: 787-93.
25. Rothman P, Coffman RL. Immunoglobulin heavy chain class-switching. In: Herzenberg LA, editor. Weir's handbook of experimental immunology. 5th ed. Oxford, United Kingdom: Blackwell Scientific Publications; 1996 p. 19.1-4.
26. Anam K, Afrin F, Banerjee D, Pramanik N, Guha SK, Goswami RP, et al. Immunoglobulin subclass distribution and diagnostic value of Leishmania donovani antigen-specific immunoglobulin G3 in Indian kala-azar patients. Clin Diagn Lab Immunol 1999; 6: 231-5.
27. Ghosh AK, Dasgupta S, Ghose AC. Immunoglobulin G subclass-specific antileishmanial antibody responses in Indian kala-azar and post-kala-azar dermal leishmaniasis. Clin Diagn Lab Immunol 1995; 2: 291-6.
28. Atta AM, D'Oliveira, Correa J, Atta ML, Almeida RP, Carvalho EM. Anti-leishmanial IgE antibodies: a marker of active disease in visceral leishmaniasis. Am J Trop Med Hyg 1998; 59: 426-30.
29. da Matta VL, Hoshino-Shimizu S, Dietze R, Corbett CE. Detection of specific antibody isotypes and subtypes before and after treatment of American visceral leishmaniasis. J Clin Lab Anal 2000; 14: 5-12.
30. Ryan JR, Smithyman AM, Rajasekariah GH, Hochberg L, Stiteler JM, Martin SK. Enzyme-linked immunosorbent assay based on soluble promastigote antigen detects immunoglobulin M (IgM) and IgG antibodies in sera from cases of visceral and cutaneous leishmaniasis. J Clin Microbiol 2002; 40: 1037-43.
31. Atta AM, Colossi R, Sousa-Atta ML, Jeronimo SM, Nascimento MD, Bezerra GF, et al. Antileishmanial IgG and IgE antibodies recognize predominantly carbohydrate epitopes of glycosylated antigens in visceral leishmaniasis. Mem Inst Oswaldo Cruz 2004; 99: 525-30.
32. Anam K, Afrin F, Banerjee D, Pramanik N, Guha SK, Goswami RP, et al. Differential decline in Leishmania membrane antigen-specific immunoglobulin G (IgG), IgM, IgE, and IgG subclass antibodies in Indian kala-azar patients after chemotherapy. Infect Immun 1999; 67: 6663-9.
33. Hailu A, Menon JN, Berhe N, Gedamu L, Hassard TH, Kager PA, et al. Distinct immunity in patients with visceral leishmaniasis from that in subclinically infected and drug-cured people: implications for the mechanism underlying drug cure. J Infect Dis 2001; 184: 112-5.
34. Miles SA, Conrad SM, Alves RG, Jeronimo SM, Mosser DM. A role for IgG immune complexes during infection with the intracellular pathogen Leishmania. J Exp Med 2005; 201: 747-54.
35. Singh S, Sivakumar R. Recent advances in the diagnosis of leishmaniasis. J Postgrad Med 2003; 49: 55-60.
36. Zijlstra EE, Khalil EAG, Kager PA, el-Hassan AM. Post-Kala-azar dermal leishmaniasis in the Sudan: clinical presentation and differential diagnosis. Br J Dermatol 2000; 143: 136-43.
37. Kubar J, Fragaki K. Recombinant DNA-derived Leishmania proteins: from the laboratory to the field. Lancet Infect Dis 2005; 5: 107-14.
38. Sundar S. Diagnosis of kala-azar - an important stride. J Assoc Physicians India 2003; 51: 753-5.
39. Sundar S, Rai M. Laboratory diagnosis of visceral leishmaniasis. Clin Diagn Lab Immunol 2002; 9: 951-8.
40. Saha S, Mazumdar T, Anam K, Ravindran R, Bairagi B, Saha B, et al. Leishmania promastigote membrane antigen-based enzyme-linked immunosorbent assay and immunoblotting for differential diagnosis of Indian post-kala-azar dermal leishmaniasis. J Clin Microbiol 2005; 43: 1269-77.
41. Burns JM Jr, Shreffler WG, Benson DR, Ghalib HW, Badaro R, Reed SG. Molecular characterization of a Kinesin-related antigen of Leishmania Chagasi that detects specific antibody in African and American visceral leishmaniasis. Proc Natl Acad Sci USA 1993; 90: 775-9.
42. Chappuis F, Rijal S, Singh R, Acharya P, Karki BM, Das ML, et al. Prospective evaluation and comparison of the direct agglutination test and an rK39-antigen-based dipstick test for the diagnosis of suspected kalaazar in Nepal. Trop Med Int Health 2003; 8: 277-85.
43. Sundar S, Reed SG, Singh VP, Kumar PC, Murray HW. Rapid accurate field diagnosis of Indian visceral leishmaniasis. Lancet 1998; 351: 563-5.
44. Sundar S, Pai K, Sahu M, Kumar V, Murray HW. Immunochromatographic strip-test detection of anti-K39 antibody in Indian visceral leishmaniasis. Ann Trop Med Parasitol 2002; 96: 19-23.
45. Singh S, Kumari V, Singh N. Predicting kala-azar disease manifestations in asymptomatic patients with latent Leishmania donovani infection by detection of antibody against recombinant K39 antigen. Clin Diagn Lab Immunol 2002; 9: 568-72.
46. Goswami RP, Bairagi B, Kundu PK. K39 strip test - easy, reliable and cost-effective field diagnosis for visceral leishmaniasis in India. J Assoc Physicians India 2003; 51: 759-61.
47. Bern C, Jha SN, Joshi AB, Thakur GD, Bista MB. Use of the recombinant K39 dipstick test and the direct agglutination test in a setting endemic for visceral leishmaniasis in Nepal. Am J Trop Med Hyg 2000; 63: 153-7.
48. Sarker CB, Momen A, Jamal MF, Siddiqui NI, Siddiqui FM, Chowdhury KS, et al. Immunochromatographic (rK39) strip test in the diagnosis of visceral leishmaniasis in Bangladesh. Mymensingh Med J 2003; 12: 93-7.
49. Zijlstra EE, Nur Y, Desjeux P, Khalil EA, El-Hassan AM, Groen J. Diagnosing visceral leishmaniasis with the recombinant K39 strip test: experience from the Sudan. Trop Med Int Health 2001; 6: 108-13.
50. Veeken H, Ritmeijer K, Seaman J, Davidson R. Comparison of an rK39 dipstick rapid test with direct agglutination test and splenic aspiration for the diagnosis of kala-azar in Sudan. Trop Med Int Health 2003; 8: 164-7.
51. Schallig HD, Canto-Cavalheiro M, da Silva ES. Evaluation of the direct agglutination test and the rK39 dipstick test for the sero-diagnosis of visceral leishmaniasis. Mem Inst Oswaldo Cruz 2002; 97: 1015-8.
52. Carvalho SF, Lemos EM, Corey R, Dietze R. Performance of recombinant K39 antigen in the diagnosis of Brazilian visceral leishmaniasis. Am J Trop Med Hyg 2003; 68: 321-4.
53. Jelinek T, Eichenlaub S, Loscher T. Sensitivity and specificity of a rapid immunochromatographic test for diagnosis of visceral leishmaniasis. Eur J Clin Microbiol Infect Dis 1999; 18: 669-70.
54. Zijlstra EE, Daifalla NS, Kager PA, Khalil EA, el-Hassan AM, Reed SG, et al. rK39 enzyme-linked immunosorbent assay for diagnosis of Leishmania donovani infection. Clin Diagn Lab Immunol 1998; 5: 717-20.
55. Badaro R, Benson D, Eulalio MC, Freire M, Cunha S, Netto EM, et al. rK39: a cloned antigen of Leishmania chagasi that predicts active visceral leishmaniasis. J Infect Dis 1996; 173: 758-61.
56. Boarino A, Scalone A, Gradoni L, Ferroglio E, Vitale F, Zanatta R, et al. Development of recombinant chimeric antigen expressing immunodominant B epitopes of Leishmania infantum for serodiagnosis of visceral leishmaniasis. Clin Diagn Lab Immunol 2005; 12: 647-53.
57. Ravindran R, Anam K, Bairagi BC, Saha B, Pramanik N, Guha SK, et al. Characterization of immunoglobulin G and its subclass response to Indian kala-azar infection before and after chemotherapy. Infect Immun 2004; 72: 863-70.
58. Boelaert M, Rijal S, Regmi S, Singh R, Karki B, Jacquet D, et al. A comparative study of the effectiveness of diagnostic tests for visceral leishmaniasis. Am J Trop Med Hyg 2004; 70: 72-7.
59. Rijal S, Boelaert M, Regmi S, Karki BM, Jacquet D, Singh R, et al. Evaluation of a urinary antigen-based latex agglutination test in the diagnosis of kala-azar in eastern Nepal. Trop Med Int Health 2004; 9: 724-9.
60. Islam MZ, Itoh M, Mirza R, Ahmed I, Ekram AR, Sarder AH, et al. Direct agglutination test with urine samples for the diagnosis of visceral leishmaniasis. Am J Trop Med Hyg 2004; 70: 78-82.
61. Abdallah KA, Nour BY, Schallig HD, Mergani A, Hamid Z, Elkarim AA, et al. Evaluation of the direct agglutination test based on freeze-dried Leishmania donovani promastigotes for the serodiagnosis of visceral leishmaniasis in Sudanese patients. Trop Med Int Health 2004; 9: 1127-31.
62. Riera C, Fisa R, Lopez P, Ribera E, Carrio J, Falco V, et al. Evaluation of a latex agglutination test (KAtex) for detection of Leishmania antigen in urine of patients with HIV-Leishmania coinfection: value in diagnosis and post-treatment follow-up. Eur J Clin Microbiol Infect Dis 2004; 23: 899-904.
63. Maalej IA, Chenik M, Louzir H, Ben Salah A, Bahloul C, Amri F, et al. Comparative evaluation of ELISAs based on ten recombinant or purified Leishmania antigens for the serodiagnosis of Mediterranean visceral leishmaniasis. Am J Trop Med Hyg 2003; 68: 312-20.
64. Salotra P, Sreenivas G, Nasim AA, Subba Raju BV, Ramesh V. Evaluation of enzyme-linked immunosorbent assay for diagnosis of post-kala-azar dermal leishmaniasis with crude or recombinant k39 antigen. Clin Diagn Lab Immunol 2002; 9: 370-3.
65. Carvalho FA, Charest H, Tavares CA, Matlashewski G, Valente EP, Rabello A, et al. Diagnosis of American visceral leishmaniasis in humans and dogs using the recombinant Leishmania donovani A2 antigen. Diagn Microbiol Infect Dis 2002; 43: 289-95.
66. Kumar P, Pai K, Tripathi K, Pandey HP, Sundar S. Immunoblot analysis of the humoral immune response to Leishmania donovani polypeptides in cases of human visceral leishmaniasis: its usefulness in prognosis. Clin Diagn Lab Immunol 2002; 9: 1119-23.
67. Attar ZJ, Chance ML, el-Safi S, Carney J, Azazy A, El-Hadi M, et al. Latex agglutination test for the detection of urinary antigens in visceral leishmaniasis. Acta Trop 2001; 78: 11-6.
68. Kaul P, Malla N, Kaur S, Mahajan RC, Ganguly NK. Evaluation of a 200-kDa amastigote-specific antigen of L. donovani by enzyme-linked immunosorbent assay (ELISA) for the diagnosis of visceral leishmaniasis. Trans R Soc Trop Med Hyg 2000; 94: 173-5.
69. Gaafar A, Kharazmi A, Ismail A, Kemp M, Hey A, Christensen CB, et al. Dichotomy of the T cell response to Leishmania antigens in patients suffering from cutaneous leishmaniasis; absence or scarcity of Th1 activity is associated with severe infections. Clin Exp Immunol 1995; 100: 239-45.
70. Manson-Bahr PE. Immunity in kala-azar. Trans R Soc Trop Med Hyg 1961; 55: 550-5.
71. Reiner SL, Locksley RM. The regulation of immunity to Leishmania major. Annu Rev Immunol 1995; 13: 151-77.
72. Carvalho EM, Teixeira RS, Johnson WD Jr. Cell-mediated immunity in American visceral leishmaniasis: reversible immunosuppression during acute infection. Infect Immun 1981; 33: 498-500.
73. Ho M, Koech DK, Iha DW, Bryceson AD. Immunosuppression in Kenyan visceral leishmaniasis. Clin Exp Immunol 1983; 51: 207-14.
74. Haldar JP, Ghose S, Saha KC, Ghose AC. Cell-mediated immune response in Indian kala-azar and post-kala-azar dermal leishmaniasis. Infect Immun 1983; 42: 702-7.
75. Neogy AB, Nandy A, Ghosh Dastidar B, Chowdhury AB. Modulation of the cell-mediated immune response in kala-azar and post-kala-azar dermal leishmaniasis in relation to chemotherapy. Ann Trop Med Parasitol 1988; 82: 27-34.
76. Koech DK. Subpopulations of T lymphocytes in Kenyan patients with visceral leishmaniasis. Am J Trop Med Hyg 1987; 36: 497-500.
77. Ribeiro-de-Jesus A, Almeida RP, Lessa H, Bacellar O, Carvalho EM. Cytokine profile and pathology in human leishmaniasis. Braz J Med Biol Res 1998; 31: 143-8.
78. Carvalho EM, Bacellar O, Brownell C, Regis T, Coffman RL, Reed SG. Restoration of IFN-gamma production and lymphocyte proliferation in visceral leishmaniasis. J Immunol 1994; 152: 5949-56.
79. Carvalho EM, Bacellar O, Barral A, Badaro R, Johnson WD Jr. Antigen-specific immunosuppression in visceral leishmaniasis is cell mediated. J Clin Invest 1989; 83: 860-4.
80. Blackwell JM, Ulczak OM. Immunoregulation of genetically controlled acquired responses to Leishmania donovani infection in mice: demonstration and characterization of suppressor T cells in noncure mice. Infect Immun 1984; 44: 97-102.
81. Cillari E, Liew FY, Lo Campo P, Milano S, Mansueto S, Salerno A. Suppression of IL-2 production by cryopreserved peripheral blood mononuclear cells from patients with active visceral leishmaniasis in Sicily. J Immunol 1988; 140: 2721-6.
82. Powrie F, Correa-Oliveira R, Mauze S, Coffman RL. Regulatory interactions between CD45RBhigh and CD45RBlow CD4+ T cells are important for the balance between protective and pathogenic cell-mediated immunity. J Exp Med 1994; 179: 589-600.
83. Heinzel FP, Sadick MD, Holaday BJ, Coffman RL, Locksley RM. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J Exp Med 1989; 169: 59-72.
84. Kemp M, Kurtzhals JA, Bendtzen K, Poulsen LK, Hansen MB, Koech DK, et al. Leishmania donovani-reactive Th1- and Th2-like T-cell clones from individuals who have recovered from visceral leishmaniasis. Infect Immun 1993; 61: 1069-73.
85. D'Oliveira Junior A, Costa SR, Barbosa AB, Orge M de la G, Carvalho EM. Asymptomatic Leishmania chagasi infection in relatives and neighbors of patients with visceral leishmaniasis. Mem Inst Oswaldo Cruz 1997; 92: 15-20.
86. Zwingenberger K, Harms G, Pedrosa C, Omena S, Sandkamp B, Neifer S. Determinants of the immune response in visceral leishmaniasis: evidence for predominance of endogenous interleukin 4 over interferon-gamma production. Clin Immunol Immunopathol 1990; 57: 242-9.
87. Bahrenscheer J, Kemp M, Kurtzhals JA, Gachihi GS, Kharazmi A, Theander TG. Interferon-gamma and interleukin-4 production by human T cells recognizing Leishmania donovani antigens separated by SDS-PAGE. APMIS 1995; 103: 131-9.
88. Carvalho EM, Badaro R, Reed SG, Jones TC, Johnson WD Jr. Absence of gamma interferon and interleukin 2 production during active visceral leishmaniasis. J Clin Invest 1985; 76: 2066-9.
89. Holaday BJ, Pompeu MM, Evans T, Braga DN, Texeira MJ, Sousa Ade Q, et al. Correlates of Leishmania-specific immunity in the clinical spectrum of infection with Leishmania chagasi. J Infect Dis 1993; 167: 411-7.
90. Murray HW, Rubin BY, Rothermel CD. Killing of intracellular Leishmania donovani by lymphokine-stimulated human mononuclear phagocytes. Evidence that interferon-gamma is the activating lymphokine. J Clin Invest 1983; 72: 1506-10.
91. Murray HW, Cartelli DM. Killing of intracellular Leishmania donovani by human mononuclear phagocytes. Evidence for oxygen-dependent and -independent leishmanicidal activity. J Clin Invest 1983; 72: 32-44.
92. Vouldoukis I, Becherel PA, Riveros-Moreno V, Arock M, da Silva O, Debre P, et al. nterleukin-10 and interleukin-4 inhibit intracellular killing of Leishmania infantum and Leishmania major by human macrophages by decreasing nitric oxide generation. Eur J Immunol 1997; 27: 860-5.
93. Ho JL, Badaro R, Schwartz A, Dinarello CA, Gelfand JA, Sobel J, et al. Diminished in vitro production of interleukin-1 and tumor necrosis factor-alpha during acute visceral leishmaniasis and recovery after therapy. J Infect Dis 1992; 165: 1094-102.
94. Barral-Netto M, Badaro R, Barral A, Almeida RP, Santos SB, Badaro F, et al. Tumor necrosis factor (cachectin) in human visceral leishmaniasis. J Infect Dis 1991; 163: 853-7.
95. Bacellar O, Barral-Netto M, Badaro R, Carvalho EM. Gamma interferon production by lymphocytes from children infected with L. chagasi. Braz J Med Biol Res 1991; 24: 791-5.
96. Nylen S, Maasho K, Soderstrom K, Ilg T, Akuffo H. Live Leishmania promastigotes can directly activate primary human natural killer cells to produce interferon-gamma. Clin Exp Immunol 2003; 131: 457-67.
97. Badaro R, Falcoff E, Badaro FS, Carvalho EM, Pedral-Sampaio D, Barral A, et al. Treatment of visceral leishmaniasis with pentavalent antimony and interferon gamma. N Engl J Med 1990; 322: 16-21.
98. Harms G, Zwingenberger K, Sandkamp B, Omena S, Pedrosa C, Richter J, et al. Immunochemotherapy of visceral leishmaniasis: a pilot trial of sequential treatment with recombinant interferon-gamma and pentavalent antimony. J Interferon Res 1993; 13: 39-41.
99. Badaro R, Johnson WD Jr. The role of interferon-gamma in the treatment of visceral and diffuse cutaneous leishmaniasis. J Infect Dis 1993; 167 (Suppl 1): S13-7.
100. Squires KE, Rosenkaimer F, Sherwood JA, Forni AL, Were JB, Murray HW. Immunochemotherapy for visceral leishmaniasis: a controlled pilot trial of antimony versus antimony plus interferon-gamma. Am J Trop Med Hyg 1993; 48: 666-9.
101. van Lunzen J, Kern P, Schmitz J, Brzoska J, Flessenkamper S, Dietrich M. Short term treatment of visceral leishmaniasis of the Old World with low dose interferon gamma and pentavalent antimony. Infection 1993; 21: 362-6.
102. Sundar S, Rosenkaimer F, Murray HW. Successful treatment of refractory visceral leishmaniasis in India using antimony plus interferon-gamma. J Infect Dis 1994; 170: 659-62.
103. Sundar S, Rosenkaimer F, Lesser ML, Murray HW. Immunochemotherapy for a systemic intracellular infection: accelerated response using interferon-gamma in visceral leishmaniasis. J Infect Dis 1995; 171: 992-6.
104. Sundar S, Murray HW. Effect of treatment with interferon-gamma alone in visceral leishman iasis. J Infect Dis 1995; 172: 1627-9.
105. Sundar S, Singh VP, Sharma S, Makharia MK, Murray HW. Response to interferon-gamma plus pentavalent antimony in Indian visceral leishmaniasis. J Infect Dis 1997; 176: 1117-9.
106. de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 1991; 174: 1209-20.
107. Oswald IP, Wynn TA, Sher A, James SL. Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proc Natl Acad Sci 1992; 89: 8676-80.
108. Holaday BJ, Pompeu MM, Jeronimo S, Texeira MJ, Sousa Ade A, Vasconcelos AW, et al. Potential role for interieukin-10 in the immunosuppression associated with kala azar. J Clin Invest 1993; 92: 2626-32.
109. Karp CL, el-Safi SH, Wynn TA, Satti MM, Kordofani AM, Hashim FA, et al. In vivo cytokine profiles in patients with kala-azar. Marked elevation of both interleukin-10 and interferon-gamma. J Clin Invest 1993; 91: 1644-8.
110. Ghalib HW, Piuvezam MR, Skeiky YA, Siddig M, Hashim FA, el-Hassan AM, et al. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J Clin Invest 1993; 92: 324-9.
111. Kenney RT, Sacks DL, Gam AA, Murray HW, Sundar S. Splenic cytokine responses in Indian kala-azar before and after treatment. J Infect Dis 1998; 177: 815-8.
112. Gasim S, Elhassan AM, Khalil EA, Ismail A, Kadaru AM, Kharazmi A, et al. High levels of plasma IL-10 and expression of IL-10 by keratinocytes during visceral leishmaniasis predict subsequent development of post-kala-azar dermal leishmaniasis. Clin Exp Immunol 1998; 111: 64-9.
113. Kobayashi M, Fitz L, Ryan M, Hewick RM, Clark SC, Chan S, et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 1989; 170: 827-45.
114. Stern AS, Podlaski FJ, Hulmes JD, Pan YC, Quinn PM, Wolitzky AG, et al. Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells. Proc Natl Acad Sci USA 1990; 87: 6808-12.
115. Trinchieri G. Interleukin-12 and its role in the generation of TH1 cells. Immunol Today 1993; 14: 335-8.
116. Scott P. IL-12: initiation cytokine for cell-mediated immunity. Science 1993; 260: 496-7.
117. Chan SH, Kobayashi M, Santoli D, Perussia B, Trinchieri G. Mechanisms of IFN-gamma induction by natural killer cell stimulatory factor (NKSF/ IL-12). Role of transcription and mRNA stability in the synergistic interaction between NKSF and IL-2. J Immunol 1992; 148: 92-8.
118. Heinzel FP, Schoenhaut DS, Rerko RM, Rosser LE, Gately MK. Recombinant interleukin 12 cures mice infected with Leishmania major. J Exp Med 1993; 177: 1505-9.
119. Sypek JP, Chung CL, Mayor SE, Subramanyam JM, Goldman SJ, Sieburth DS, et al. Resolution of cutaneous leishmaniasis: interleukin 12 initiates a protective T helper type 1 immune response. J Exp Med 1993; 177: 1797-802.
120. Ghalib HW, Whittle JA, Kubin M, Hashim FA, el-Hassan AM, Grabstein KH, et al. IL-12 enhances Th1-type responses in human Leishmania donovani infections. J Immunol 1995; 154: 4623-9.
121. Bacellar O, Brodskyn C, Guerreiro J, Barral-Netto M, Costa CH, Coffman RL, et al. Interleukin-12 restores interferon-gamma production and cytotoxic responses in visceral leishmaniasis. J Infect Dis 1996; 173: 1515-8.
122. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, Trinchieri G. Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/ IL-12 synthesis in accessory cells. J Exp Med 1993; 178 : 1041-8.
123. Bacellar O, D'oliveira A Jr, Jeronimo S, Carvalho EM. L-10 and IL-12 are the main regulatory cytokines in visceral leishmaniasis. Cytokine 2000; 12: 1228-31.
124. Mathur RK, Awasthi A, Wadhone P, Ramanamurthy B, Saha B. Reciprocal CD40 signals through p38MAPK and ERK-1/2 induce counteracting immune responses. Nat Med 2004; 10: 540-4.
125. Mary C, Auriault V, Faugere B, Dessein AJ. Control of Leishmania infantum infection is associated with CD8(+) and gamma interferon- and interleukin-5-producing CD4(+) antigen-specific T cells. Infect Immun 1999; 67: 5559-66.
126. Holaday BJ. Role of CD8+ T cells in endogenous interleukin-10 secretion associated with visceral leishmaniasis. Mem Inst Oswaldo Cruz 2000; 95: 217-20.
127. Holaday BJ. Immunotherapy for visceral leishmaniasis: ability of factors produced during anti-leishmania responses of skin test positive adults to inhibit peripheral blood mononuclear cell activities associated with visceral leishmaniasis. Mem Inst Oswaldo Cruz 1999; 94: 55-66.
128. Harrison LH, Naidu TG, Drew JS, de Alencar JE, Pearson RD. Reciprocal relationships between undernutrition and the parasitic disease visceral leishmaniasis. Rev Infect Dis 1986; 8: 447-53.
129. Kemp M, Hansen MB, Theander TG. Recognition of Leishmania antigens by T lymphocytes from nonexposed individuals. Infect Immun 1992; 60: 2246-51.
130. Kurtzhals JA, Kemp M, Poulsen LK, Hansen MB, Kharazmi A, Theander TG. Interleukin-4 and interferon-gamma production by Leishmania stimulated peripheral blood mononuclear cells from nonexposed individuals. Scand J Immunol 1995; 41: 343-9.
131. Kemp K, Hviid L, Kharazmi A, Kemp M. Interferon-gamma production by human T cells and natural killer cells in vitro in response to antigens from the two intracellular pathogens Mycobacterium tuberculosis and Leishmania major. Scand J Immunol 1997; 46: 495-9.
132. Akuffo HO, Britton SF. Contribution of non-Leishmania-specific immunity to resistance to Leishmania infection in humans. Clin Exp Immunol 1992; 87: 58-64.
133. Akuffo H, Schurr E, Andersson G, Yamaneberhan T, Britton S. Responsiveness in diffuse versus local cutaneous leishmaniasis is due to parasite differences. Scand J Immunol 1987; 26: 717-21.
134. Maasho K, Akuffo HO. Cells from healthy non-exposed individuals produce cytokines to selected fractions of Leishmania promastigotes. Scand J Immunol Suppl 1992; 11: 179-84.
135. Kurtzhals JA, Hey AS, Jardim A, Kemp M, Schaefer KU, Odera EO, et al. Dichotomy of the human T cell response to Leishmania antigens. II. Absent or Th2-like response to gp63 and Th1-like response to lipophosphoglycan-associated protein in cells from cured visceral leishmaniasis patients. Clin Exp Immunol 1994; 96: 416-21.
136. Kemp K, Kemp M, Kharazmi A, Ismail A, Kurtzhals JA, Hviid L, et al. Leishmania-specific T cells expressing interferon-gamma (IFN-gamma) and IL-10 upon activation are expanded in individuals cured of visceral leishmaniasis. Clin Exp Immunol 1999; 116: 500-4.
137. Maasho K, McMahon-Pratt D, Raita J, Raud M, Britton S, Soong L, et al. Evaluation of amastigote reactive cells in human cutaneous leishmaniasis caused by Leishmania aethiopica. Clin Exp Immunol 2003; 132: 316-22.
138. Akuffo H, Maasho K, Howe R. Natural and acquired resistance to Leishmania: cellular activation by Leishmania aethiopica of mononuclear cells from unexposed individuals is through the stimulation of natural killer (NK) cells. Clin Exp Immunol 1993; 94: 516-21.
139. Maasho K, Satti I, Nylen S, Guzman G, Koning F, Akuffo H. A Leishmania homologue of receptors for activated C-kinase (LACK) induces both interferon-gamma and interleukin-10 in natural killer cells of healthy blood donors. J Infect Dis 2000; 182: 570-8.
140. Sundar S, Reed SG, Sharma S, Mehrotra A, Murray HW. Circulating T helper 1 (Th1) cell- and Th2 cell-associated cytokines in Indian patients with visceral leishmaniasis. Am J Trop Med Hyg 1997; 56: 522-5.
141. Kemp M, Hey AS, Kurtzhals JA, Christensen CB, Gaafar A, Mustafa MD, et al. Dichotomy of the human T cell response to Leishmania antigens. I. Th1-like response to Leishmania major promastigote antigens in individuals recovered from cutaneous leishmaniasis. Clin Exp Immunol 1994; 96: 410-5.
142. Sang DK, Ouma JH, John CC, Whalen CC, King CL, Mahmoud AA, et al. Increased levels of soluble interleukin-4 receptor in the sera of patients with visceral leishmaniasis. J Infect Dis 1999; 179: 743-6.
143. Babaloo Z, Kaye PM, Eslami MB. Interleukin-13 in Iranian patients with visceral leishmaniasis: relationship to other Th2 and Th1 cytokines. Trans R Soc Trop Med Hyg 2001; 95: 85-8.
144. Gantt KR, Goldman TL, McCormick ML, Miller MA, Jeronimo SM, Nascimento ET, et al. Oxidative responses of human and murine macrophages during phagocytosis of Leishmania chagasi. J Immunol 2001; 167: 893-901.
145. Nascimento ET, Gantt KR, Pontes N, Bacelar O, Luz VE, Wilson ME, et al. TGF-β in acute visceral leishmaniasis. Am J Trop Med Hyg 2002; 67: 262.
146. Gantt KR, Schultz-Cherry S, Rodriguez N, Jeronimo SM, Nascimento ET, Goldman TL, et al. Activation of TGF-beta by Leishmania chagasi: importance for parasite survival in macrophages. J Immunol 2003; 170: 2613-20.
147. Gurunathan S, Prussin C, Sacks DL, Seder RA. Vaccine requirements for sustained cellular immunity to an intracellular parasitic infection. Nat Med 1998; 4 : 1409-15.
148. Kimsey PB, Theodos CM, Mitchen TK, Turco SJ, Titus RG. 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: 5205-13.
149. Sharifi I, Fekri AR, Aflatonian MR, Khamesipour A, Nadim A, Mousavi MRA, et al. Randomised vaccine trial of single dose of killed Leishmania major plus BCG against anthroponotic cutaneous leishmaniasis in Bam, Iran. Lancet 1998; 351: 1540-3.
150. Sjolander A, Baldwin TM, Curtis JM, Handman E. Induction of Th1 immune response and simultaneous lack of activation of a Th2 response are required for generation of immunity to leishmaniasis. J Immunol 1998; 160: 3949-57.
151. Bouvier J, Etges R, Bordier C. Identification of the promastigote surface protease in seven species of Leishmania. Mol Biochem Parasitol 1987; 24: 73-9.
152. Colomer-Gould V, Glvao Quintao L, Keithly J, Nogueira N. A common major surface antigen on amastigotes and promastigotes of Leishmania species. J Exp Med 1985; 162 : 902-16.
153. Handman E, Greenblatt CL, Goding JW. An amphipathic sulphated glycoconjugate of Leishmania: characterization with monoclonal antibodies. EMBO J 1984; 3: 2301-6.
154. Orlandi PA Jr, Turco SJ. Structure of the lipid moiety of the Leishmania donovani lipophosphoglycan. J Biol Chem 1987; 262: 10384-91.
155. Turco SJ, Hull SR, Orlandi PA Jr, Shepherd SD, Homans SW, Dwek RA, et al. Structure of the major carbohydrate fragment of the Leishmania donovani lipophosphoglycan. Biochemistry 1987; 26: 6233-8.
156. Mendonca SC, Russell DG, Coutinho SG. Analysis of the human T cell responsiveness to purified antigens of Leishmania: lipophosphoglycan (LPG) and glycoprotein 63 (gp 63). Clin Exp Immunol 1991; 83 : 472-8.
157. Russell DG, Alexander J. Effective immunization against cutaneous leishmaniasis with defined membrane antigens reconstituted into liposomes. J Immunol 1988; 140 : 1274-9.
158. Kemp M, Theander TG, Handman E, Hey AS, Kurtzhals JA, Hviid L, et al. Activation of human T lymphocytes by Leishmania lipophosphoglycan. Scand J Immunol 1991; 33 : 219-24.
159. Kemp M, Hey AS, Bendtzen K, Kharazmi A, Theander TG. Th1-like human T-cell clones recognizing Leishmania gp63 inhibit Leishmania major in human macrophages. Scand J Immunol 1994; 40: 629-35.
160. Kemp M, Kurtzhals JA, Christensen CB, Kharazmi A, Jardim A, Bendtzen K, et al. Production of interferon-gamma and interleukin-4 by human T cells recognizing Leishmania lipophosphoglycan-associated protein. Immunol Lett 1993; 38 : 137-44.
161. Kemp M, Handman E, Kemp K, Ismail A, Mustafa MD, Kordofani AY, et al. The Leishmania promastigote surface antigen-2 (PSA-2) is specifically recognised by Th1 cells in humans with naturally acquired immunity to L. major. FEMS Immunol Med Microbiol 1998; 20: 209-18.
162. Kurtzhals JA, Hansen MB, Hey AS, Poulsen LK. Measurement of antigen-dependent interleukin-4 production by human peripheral blood mononuclear cells. Introduction of an amplification step using ionomycin and phorbol myristate acetate. J Immunol Methods 1992; 156 : 239-45.
163. Khalil EA, Ayed NB, Musa AM, Ibrahim ME, Mukhtar MM, Zijlstra EE, et al. Dichotomy of protective cellular immune responses to human visceral leishmaniasis. Clin Exp Immunol 2005; 140 : 349-53.
164. Jensen AT, Gasim. S, Ismail A, Gaafar A, Kurtzhals JA, Kemp M, et al. Humoral and cellular immune responses to synthetic peptides of the Leishmania donovani kinetoplastid membrane protein-11. Scand J Immunol 1998; 48 : 103-9.
165. Symons FM, Murray PJ, Ji H, Simpson RJ, Osborn AH, Cappai R, et al. Characterization of a polymorphic family of integral membrane proteins in promastigotes of different Leishmania species. Mol Biochem Parasitol 1994; 67: 103-13.
166. Skeiky YA, Guderian JA, Benson DR, Bacelar O, Carvalho EM, Kubin M, et al. A recombinant Leishmania antigen that stimulates human peripheral blood mononuclear cells to express a Th1-type cytokine profile and to produce interleukin 12. J Exp Med 1995; 181 : 1527-37.
167. Russo DM, Chakrabarti P, Higgins AY. Leishmania: naive human T cells sensitized with promastigote antigen and IL-12 develop into potent Th1 and CD8(+) cytotoxic effectors. Exp Parasitol 1999; 93 : 161-70.
168. Costa SR, D'Oliveira A Jr, Bacellar O, Carvalho EM. T cell response of asymptomatic Leishmania chagasi infected subjects to recombinant Leishmania antigens. Mem Inst Oswaldo Cruz 1999; 94 : 367-70.
169. Suffia I, Ferrua B, Stien X, Mograbi B, Marty P, Rousseau D, et al. A novel Leishmania infantum recombinant antigen which elicits interleukin 10 production by peripheral blood mononuclear cells of patients with visceral leishmaniasis. Infect Immun 2000; 68 : 630-6.
170. Julia V, Rassoulzadegan M, Glaichenhaus N. Resistance to Leishmania major induced by tolerance to a single antigen. Science 1996; 274 : 421-3.
171. Maasho K, Wolday D, Edjigu M, Soderstrom K, Britton S, Akuffo H. Induction and abrogation of LACK reactive cells in the evolution of human leishmaniasis. Clin Exp Immunol 2001; 124 : 255-61.
172. Bourreau E, Collet M, Prevot G, Milon G, Ashimoff D, Hasagewa H, et al. IFN-gamma-producing CD45RA+CD8+ and IL-10-producing CD45RA-CD4+ T cells generated in response to LACK in naive subjects never exposed to Leishmania. Eur J Immunol 2002; 32: 510-20.
173. Pintado V, Lopez-Velez R. HIV-associated visceral leishmaniasis. Clin Microbiol Infect 2001; 7: 291-300.
174. Desjeux P, Alvar J. Leishmania/HIV co-infections: epidemiology in Europe. Ann Trop Med Parasitol 2003; 97 (Suppl 1) : 3-15.
175. Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, Desjeux P, et al. Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet Infect Dis 2002; 2 : 494-501.
176. Wolday D, Berhe N, Akuffo H, Desjeux P, Britton S. Emerging Leishmania/ HIV co-infection in Africa. Med Microbiol Immunol 2001; 190: 65-7.
177. Bernier R, Turco SJ, Olivier M, Tremblay M. Activation of human immunodeficiency virus type 1 in monocytoid cells by the protozoan parasite Leishmania donovani. J Virol 1995; 69: 7282-5.
178. Wolday D, Akuffo H, Britton S, Hathaway A, Sander B. HIV-1 inhibits Leishmania-induced cell proliferation but not production of interleukin-6 and tumour necrosis factor alpha. Scand J Immunol 1994; 39: 380-6.
179. Wolday D, Akuffo H. Demissie A, Britton S. Role of Leishmania donovani and its lipophosphoglycan in CD4+ T-cell activation-induced human immunodeficiency virus replication. Infect Immun 1999; 67: 5258-64.
180. Wolday D, Akuffo H, Fessahaye G, Valantine A, Britton S. Live and killed human immunodeficiency virus type-1 increases the intracellular growth of Leishmania donovani in monocyte-derived cells. Scand J Infect Dis 1998; 30 : 29-34.
181. Wolday D, Berhe N, Britton S, Akuffo H. HIV-1 alters T helper cytokines, interleukin-12 and interleukin-18 responses to the protozoan parasite Leishmania donovani. AIDS 2000; 14: 921-9.
182. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995; 155 : 1151-64.
183. Sakaguchi S. Regulatory T cells: key controllers of immunologic self-tolerance. Cell 2000; 101 : 455-8.
184. Belkaid Y. The role of CD4(+)CD25(+) regulatory T cells in Leishmania infection. Expert Opin Biol Ther 2003; 3 : 875-85.
185. McHugh RS, Whitters MJ, Piccirillo CA, Young DA, Shevach EM, Collins M, et at. CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 2002; 16 : 311-23.
186. Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 2002; 3 : 135-42.
187. Caramalho I, Lopes-Carvalho T, Ostler D, Zelenay S, Haury M, Demengeot J. Regulatory T cells selectively express toll-like receptors and are activated by lipopolysaccharide. J Exp Med 2003; 197: 403-11.
188. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002; 420 : 502-7.
189. Xu D, Liu H, Komai-Koma M, Campbell C, McSharry C, Alexander J, et al. CD4+CD25+ regulatory T cells suppress differentiation and functions of Th1 and Th2 cells, Leishmania major infection, and colitis in mice. J Immunol 2003; 170 : 394-9.
190. Brahmachari UN. A new form of cutaneous leishmaniasis - dermal leishmanoid. Indian Med Gaz 1922; 57: 125.
191. Thakur CP, Kumar K. Post kala-azar dermal leishmaniasis: a neglected aspect of kala-azar control programmes. Ann Trop Med Parasitol 1992; 86: 355-9.
192. Zijlstra EE, Musa AM, Khalil EA, el-Hassan IM, el-Hassan AM. Post-kala-azar dermal leishmaniasis. Lancet Infect Dis 2003; 3 : 87-98.
193. Zijlstra EE, el-Hassan AM. Leishmanin and tuberculin sensitivity in leishmaniasis in the Sudan, with special reference to kala-azar. Trans R Soc Trop Med Hyg 1993; 87 : 425-7.
194. Neogy AB, Nandy A, Ghosh Dastidar B, Chowdhury AB. Modulation of the cell-mediated immune response in kala-azar and post-kala-azar dermal leishmaniasis in relation to chemotherapy. Ann Trop Med Parasitol 1988; 82 : 27-34.
195. Ismail A, El Hassan AM, Kemp K, Gasim S, Kadaru AE, Moller T, et al. Immunopathology of post kala-azar dermal leishmaniasis (PKDL): T-cell phenotypes and cytokine profile. J Pathol 1999; 189: 615-22.
196. Ghosh MK, Nandy A, Addy M, Maitra TK, Ghose AC. Subpopulations of T lymphocytes in the peripheral blood, dermal lesions and lymph nodes of post kala-azar dermal leishmaniasis patients. Scand J Immunol 1995; 41 : 11-7.
197. Rathi SK, Pandhi RK, Chopra P, Khanna N. Lesional T-cell subset in post-kala-azar dermal leishmaniasis. Int J Dermatol 2005; 44 : 12-3.
198. Modlin RL, Tapia FJ, Bloom BR, Gallinoto ME, Castes M, Rondon AJ, et al. In situ characterization of the cellular immune response in American cutaneous leishmaniasis. Clin Exp Immunol 1985; 60 : 241-8.