HTLV-1 modifies the clinical and immunological response to schistosomiasis
A. F. PORTO
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorS. B. SANTOS
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorL. ALCÂNTARA
Laboratório de Parasitologia, Faculdade de Farmácia, Universidade Federal da Bahia and
Search for more papers by this authorJ. B. GUERREIRO
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorJ. PASSOS
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorT. GONZALEZ
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorD. GONZALEZ
Clínica de Ultrassonografia Delfin, Salvador, Bahia, Brazil,
Search for more papers by this authorCorresponding Author
E. M. CARVALHO
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Dr Carvalho, Hospital Universitário Prof Edgard Santos, Laboratório de Imunologia − 5° andar, Rua João das Botas s/n-Canela 40110–160, Salvador, Bahia, Brazil. E-mail: [email protected]Search for more papers by this authorA. F. PORTO
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorS. B. SANTOS
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorL. ALCÂNTARA
Laboratório de Parasitologia, Faculdade de Farmácia, Universidade Federal da Bahia and
Search for more papers by this authorJ. B. GUERREIRO
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorJ. PASSOS
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorT. GONZALEZ
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Search for more papers by this authorD. GONZALEZ
Clínica de Ultrassonografia Delfin, Salvador, Bahia, Brazil,
Search for more papers by this authorCorresponding Author
E. M. CARVALHO
Serviço de Imunologia do Hospital Unversitário Prof Edgard Santos and
Dr Carvalho, Hospital Universitário Prof Edgard Santos, Laboratório de Imunologia − 5° andar, Rua João das Botas s/n-Canela 40110–160, Salvador, Bahia, Brazil. E-mail: [email protected]Search for more papers by this authorSUMMARY
The immunological response in HTLV-1 infected individuals is characterized by a prominent Type-1 cytokine response with high production of IFN-γ and TNF-α. In contrast, helminthic infections and in particular chronic schistosomiasis are associated with a predominant production of IL-4, IL-5, IL-10 and IL-13. Liver fibrosis is the main pathological finding in schistosomiasis that occurs after many years of infection. This pathology is T cell dependent but the immune response mechanisms are not completely understood. The North-east region of Brazil is endemic for both HTLV-1 and schistosomiasis. In the present study the immune response, clinical severity, and therapeutic response to praziquantel of patients with schistosomiasis coinfected with HTLV-1 were compared with patients infected only with S. mansoni. Patients with HTLV-1 and S. mansoni had lower levels of IL-5 (P < 0·05) and higher levels of IFN-γ (P < 0·05) in cultures stimulated with S. mansoni antigen and decreased S. mansoni antigen specific IgE levels when compared with patients with schistosomiasis without HTLV-1 coinfection. Liver fibrosis was mild in all HTLV-1 coinfected patients and efficacy of praziquantel was lower in patients dually infected than in patients infected only with S. mansoni.
REFERENCES
- 1 Edlich RF, Arnette JA, Williams FM. Global epidemic of human T-cell lymphotropic virus type-I (HTLV-I). J Emerg Med 2000; 18: 109 – 19.
- 2 Carvalho EM, Bacellar O, Porto MAF, Santos SB, Galvão-Castro B, Neva FA. Cytokine Profile and Immunomodulation In Asymptomatic HTLV-1 Infected Blood Donors. J Acquir Immune Defic Syndr Hum Retrov 2001; 26: 1 – 6.
- 3 Goon PKC, Igakura T, Hanon E, Mosley AJ, Gould BAKG. High Circulating Frequencies of Tumor Necrosis Factor Alpha-and Interleukin-2-Secreting Human T-lymphotropic Virus Type 1-Specific CD4+ T cells in Patients with HTLV-1-Associated Neurological Disease. J Virol 2003; 77: 9716 – 22.
- 4
Kramer A,
Jacobson S,
Reuben JF.
Spontaneous lymphocyte proliferation is elevated in asymptomatic HTLV-1 positive Jamaicans.
Lancet
1989; 8668: 923
–
4.
10.1016/S0140-6736(89)91591-2 Google Scholar
- 5 Araujo MI, De Jesus AR, Bacellar O, Sabin E, Pearce E, Carvalho EM. Evidence of a T helper type-2 activation in human schistosomiasis. Eur J Immunol 1996; 26: 1399 – 403.
- 6 Finkelman FD, Donohue TS, Goldhill J. Cytokine Regulation of Host Defense Against Parasitic Gastrointestinal Nematodes. Annu Rev Immunol 1997; 15: 505 – 33.
- 7 De Jesus AR, Miranda DG, Miranda RG, Araujo I, Magalhaes A, Bacellar M, Carvalho EM. Morbidity associated with Schistosoma mansoni infection determined by ultrasound in an endemic area of Brazil, Caatinga do Moura. Am J Trop Med Hyg 2000; 63: 1 – 4.
- 8 Robinson RD, Lindo JF, Neva FA, Gam AA, Vogel P, Terry SI, Cooper ES. Immunoepidemiologic studies of strongyloides stercolalis and human T lymphtropic virus type I infections in Jamaica. J Inf Dis 1994; 169: 692 – 6.
- 9 Plumelle Y, Edouard A. Strongyloides stercoralis in T-cell leukemia/lymphoma in adults and acquired immunodeficiency syndrome. Rev Med Interne 1996; 17: 125 – 9.
- 10 Hayashi J, Kishihara Y, Yoshimura E, Furusyo N, Yamaji K, Kawakami T, Murakami H, Kashiwagi S. Correlation between human T cell lymphotropic virus type-1 and Strongyloides stercoralis infections and serum immunoglobulin E reponses in residents of Okinawa. Japan Am J Trop Med Hyg 1997; 56: 71 – 5.
- 11 Porto MAF, Neva FA, Lisboa W, Thompson R, Alcântara L, Carvalho EM. htlv-1 decreases Th2 type of immune response in patients with strongyloidiasis. Parasite Immunol 2001; 23: 503 – 7.
- 12 Neva FA, Filho JO, Gam AA, Thompson R, Freitas V, Carvalho EM. Interferon-γ and Interleukin-4 Responses in Relation to Serum IgE Levels in Persons Infected with Human T Lymphotropic Virus Type I and Strongyloides stercoralis. J Infect Dis 1998; 178: 1856 – 9.
- 13 Porto MAF, Oliveira Filho J, Neva FA, Orge G, Alcântara L, Gam A, Carvalho EM. Influence of HTLV-1 infection on the serological and Skin Test for strongyloidiasis. Am J Trop Med Hyg 2001; 65: 610 – 3.
- 14 Phelps KR, Ginsberg SS, Cinningham AW, Tschachler E, Dosik H. Case report: adult T-cell leukemia/ lymphoma associated with recurrent strongyloides hyperinfection. Am J Med Sci 1991; 302: 224 – 8.
- 15 Newton RC, Limpuangthip P, Greenberg S, Gam A, Neva FA. Strongyloides stercoralis hyperinfection in a carrier of HTLV-I virus with evidence of selective immunosuppression. Am J Med 1992; 92: 202 – 7.
- 16 Patey O, Gessain A, Breuil J et al. Seven years of recurrent severe strongyloidiasis in an HTLV-I-infected man who developed adult T-cell leukaemia. AIDS 1992; 6: 575 – 9.
- 17 Galvão CB, Loures L, Rodrigues LGM. Geographic distribution of human T-lymphotropic virus type-I among blood donors: a Brazilian nation wide study. Transfusion 1997; 37: 242.
- 18 Katz N, Chaia G. Cropological diagnosis of schistosomiasis. I. Evaluation of quantitative techniques. Rev Inst Med Trop São Paulo 1968; 10: 295 – 8.
- 19 Abdel-Wahab MF, Esmat G, Farrag A, El-Boraey YA, Strickland GT. Grading of hepatic schistosomiasis by the use of ultrasonography. Am J Trop Med Hyg 1992; 46: 403 – 8.
- 20 Umehara F, Izumo S, Ronquillo AT, Matsumuro K, Sato E, Osame M. Cytokine expression in the spinal cord lesions in HTLV-1-associated myelopathy. J Neuropathol Exp Neurol 1994; 53: 72 – 7.
- 21 Furuya T, Nakamura T, Fujimoto T et al. Elevated levels of interleukin-12 and interferon-gamma in patients with human T lymphotropic virus type I-associated myelopathy. J Neuroimmunol 1999; 95: 185 – 9.
- 22 Sleigh AC, Mott KE, Silva JT et al. A three-year follow-up of chemotherapy with oxamniquine in Brazilian community with endemic schistosomiasis mansoni. Trans R Soc Trop Med Hyg 1981; 75: 234 – 8.
- 23 Dessein AJ, Begley M, Demeure C et al. Human resistance to Schistosoma mansoni is associated with reactivity to a 37-kDa larval surface antigen. J Immunol 1988; 140: 2727 – 36.
- 24 Leptak CL, McKerrow JH. Schistosome Egg Granulomas and Hepatic Expression of TNF-α Are Dependent on Immune Priming Parasite Maturation. J Immunol 1997; 158: 301 – 7.
- 25 Chiaramonte MG, Donaldson DD, Cheever AW, Wynn TA. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J Clin Invest 1999; 104: 777 – 85.
- 26 Chiaramonte MG, Schopf LR, Neben TY, Cheever AW, Wynn T. IL-13 is a Key Regulatory Cytokine for Th2 Cell-Mediated Pulmonary Granuloma Formation and IgE Responses Induced by Schistosoma mansoni Eggs. J Immunol 1999; 162: 920 – 30.
- 27 Jankovic D, Kulberg MC, Noben-Trauth N, Caspar P, Ward JM, Cheever AW, Paul WE, Sher A. Schistosome-Infected IL-4 receptor Knockout (KO) Mice, in Contrast to IL-4 KO Mice, Fail to Develop Granulomatous Pathology While Maintainig the Same Lymphokine Expression Profile. J Immunol 1999; 163: 337 – 42.
- 28 Wynn TA, Eltoum I, Oswald IP, Cheever AW, Sher A. Endogenous interleukin-12 (IL-12) regulates granuloma formation induced by eggs of Schistosoma mansoni and exogeneous IL-12 both inhibits and prophylatically immunizes against egg pathology. J Exp Med 1994; 179: 1551 – 61.
- 29 Rezende SA, Oliveira VR, Silva AM, Alves JB, Góes-Reis LFL. Mice Lacking the Gamma Interferon Receptor Have an Impaired Granulomatous Reaction to Shistosoma mansoni Infection. Infect Immun 1997; 65: 3457 – 61.
- 30 Karanja DM, Colley DG, Nahlen BL, Ouma JH, Secor WE. Studies on schistosomiasis in western Kenya. I. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. Am J Trop Med Hyg 1997; 56: 515 – 21.
- 31 Jesus AM, Almeida RP, Bacellar O, Araujo MI, Demeure C, Bina J, Dessein A, Carvalho EM. Correlation between cell-mediated immunity and degree of infection in subjects living in na endemic area of schistosomiasis. Eur J Immunol 1993; 23: 152 – 8.
- 32 Correa-Oliveira REJ, Pearce GC, Oliveira DB et al. The human immune response to defined immunogens of Schistosoma mansoni: elevated antibody levels to paramyosin in stool-negative individuals from two endemic areas in Brazil. Trans R Soc Trop Med Hyg 1989; 83: 798 – 804.
- 33 Ribeiro de Jesus A, Araujo I, Bacellar O, Magalhaes A, Pearce E, Harn D, Strand M, Carvalho EM. Human immune responses to Schistosoma mansoni vaccine candidate antigens. Infect Immun 2000; 68: 2797 – 803.
- 34 Gotuzzo E, Terashima A, Alvarez H. Strongyloides Stercoralis Hyperinfection Associated with Human T Cell Lymphotropic Virus Type-1Infection in Peru. Am J Trop Med Hyg 1999; 60: 146 – 9.
- 35 Pagliuca A. Strongyloides hyperinfection in adult t-cell leukaemia/lymphoma. Br J Haematol 1999; 105: 1.
- 36 Dunne DW, Butterworth AE, Fulford AJ, Ouma JH, Sturrock RF. Human IgE responses to Schistosoma mansoni and resistance to reinfection. Mem Inst Oswaldo Cruz 1992; 87: 99 – 103.
- 37 Caldas IR, Correa-Oliveira R, Colosimo E, Carvalho OS, Massara CL, Colley DG, Gazzinelli G. Susceptibility and resistance to Schistosoma mansoni reinfection. parallel cellular and isotypic immunologic assessment. Am J Trop Med Hyg 2000; 62: 57 – 64.
- 38 Satoh M, Toma H, Sato Y, Takara M, Shiroma Y, Kiyuna S, Hirayama K. Reduced efficacy of treatment of strongyloidiasis in HTLV-1 carriers related to enhanced expresión of IFN-γ and TGF-β1. Clin Exp Immunol 2002; 127: 354 – 9.
- 39 Shikiya K, Zaha O, Niimura S, Uehara T, Ohshiro J, Kinjo F, Saito A, Asato R. Clinical study on ivermectin against 125 strongyloidiasis patients. Kansenshogaku Zasshi 1994; 68: 13 – 20.
