Effect of chemotherapy with praziquantel on the production of cytokines and morbidity associated with schistosomiasis mansoni

Antimicrobial Agents and Chemotherapy

Volumn 52, Issue 8, 2008, Pages 2780-2786

  Martins Leite, P ^a   Gazzinelli, G ^b,c   Alves Oliveira, L F ^a   Gazzinelli, A ^d   Malaquias, L C C ^a   Correa Oliveira, R ^b   Teixeira Carvalho, A ^b   Silveira, A M S ^a  

^a UNIVERSIDADE VALE DO RIO DOCE   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c Santa Casa de Misericordia de Goiania   (Brazil)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; PRAZIQUANTEL; SOLUBLE EGG ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; AGED; ARTICLE; CHEMOTHERAPY; CLINICAL TRIAL; CYTOKINE PRODUCTION; ECHOGRAPHY; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LIVER FIBROSIS; MAJOR CLINICAL STUDY; MALE; MORBIDITY; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; ANTHELMINTICS; BRAZIL; CYTOKINES; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-13; INTERLEUKIN-4; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; PRAZIQUANTEL; SCHISTOSOMIASIS MANSONI; TRANSFORMING GROWTH FACTOR BETA; YOUNG ADULT;

EID: 48749091288     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00173-08     Document Type: Article

References (48)

1. Abdel-Wahab, M. F., G. Esmat, A. Farrag, Y. A. el-Boraey, and G. T. Strickland. 1992. Grading of hepatic schistosomiasis by the use of ultrasonography. Am. J. Trop. Med. Hyg. 46:403-408.
2. Alves-Oliveira, L. F., E. C. Moreno, G. Gazzinelli, O. A. Martins-Filho, A. M. S. Silveira, A. Gazzinelli, L. C. C. Malaquias, P. LoVerde, P. Martins Leite, and R. Correa-Oliveira. 2006. Cytokine production associated with periportal fibrosis during chronic schistosomiasis mansoni in humans. Infect. Immun. 74:1215-1221.
3. Andrade, Z. A., A. Baptista, and T. S. Santana. 2006. Remodeling of hepatic vascular changes after specific chemotherapy of schistosomal periportal fibrosis. Mem. Inst. Oswaldo Cruz 101(Suppl. I):267-272.
4. Andrade, Z. A., and J. A. Grimaud. 1986. Evolution of the schistosomal hepatic lesions in mice after curative chemotherapy. AJP 124:59-65.
5. Arap Siongok, T. K., A. A. Mahmoud, J. H. Ouma, K. S. Warren, A. S. Muller, A. K. Handa, and H. B. Houser. 1976. Morbidity in schistosomiasis mansoni in relation to intensity of infection: study of a community in machacos, Kenya. Am. J. Trop. Med. Hyg. 25:273-284.
6. Boisier, P., C.-E. Ramarokoto, V. E. Ravaoalimalala, L. Rabarijaona, J. Serieye, J. Roux, and P. Esterre. 1998. Reversibility of Schistosoma mansoni-associated morbidity after yearly mass praziquantel therapy: ultrasonographic assessment. Trans. Royal Soc. Trop. Med. Hyg. 92:451-453.
7. Booth, M., J. K. Mwatha, S. Joseph, F. M. Jones, H. Kadso, E. Ireri, F. Kazibwe, J. Kemijumbi, C. Kariuki, G. Kimani, J. H. Ouma, N. B. Kabatereine, B. J. Vennervald, and D. W. Dunne. 2004. Periportal fibrosis in human Schistosoma mansoni infection is associated with low IL-10, low IFN-γ, high TNF-α, or low RANTES, depending on age and gender. J. Immunol. 172:1295-1303.
8. Boros, D. L., and K. S. Warren. 1970. Delayed hypersensitivity- type granuloma formation and dermal reaction induced and elicited by a soluble factor isolates from Schistosoma mansoni eggs. J. Exp. Med. 132:488-506.
9. Botros, S., H. Sayed, H. El-Dusoki, H. Sabry, I. Rabie, M. El-Ghannam, M. Hassanein, Y. A. El-Wahab, and D. Engels. 2005. Efficacy of Mirazid in comparison with praziquantel in Egyptian Schistosoma mansoni-infected school children and households. Am. J. Trop. Med. Hyg. 72:119-123.
10. Chiaramonte, M. G., A. W. Cheever, J. D. Malley, D. D. Donaldson, and T. A. Wynn. 2001. Studies of murine schistosomiasis reveal interleukin-13 blockade as a treatment for established and progressive liver fibrosis. Hepatology 34:273-282.
11. Cioli, D. 1998. Chemotherapy of schistosomiasis: an update. Parasitol. Today 14:418-422.
12. Cota, G. F., R. A. Pinto-Silva, C. M. F. Antunes, and J. R. Lambertucci. 2006. Ultrasound and clinical investigation of hepatosplenic schistosomiasis: evaluation of splenomegaly and liver fibrosis four years after mass chemotherapy with oxamniquine. Am. J. Trop. Hyg. 74:103-107.
13. Czaja, M. J., F. R. Weiner, S. Takahashi, M. A. Giambrone, P. H. van der Meide, H. Schellekens, L. Biempica, and M. A. Zern. 1989. γ-Interferon treatment inhibits collagen deposition in murine schistosomiasis. Hepatology 10:795-800.
14. Dessein, A., B. Kouriba, C. Eboumbou, H. Dessein, L. Argiro, S. Marquet, N. E. M. A. Elwali, V. Rodrigues, Y. Li, O. Doumbo, and C. Chevillard. 2004. Interleukin-13 in the skin and interferon-γ in the liver are key players in immune protection in human schistosomiasis. Immunol. Rev. 201:180-190.
15. Dessein, A. J., D. Hillaire, N. E. M. A. Elwali, S. Marquet, Q. Mahamed-Ali, A. Mirghani, S. Henri, A. A. Abdelhameed, O. K. Saeed, M. M. A. Magzoub, and L. Abel. 1999. Severe hepatic fibrosis in Schistosoma mansoni infection is controlled by a major locus that is closely linked to the interferon-gamma receptor gene. Am. J. Hum. Genet. 65:699-713.
16. Doehring-Schwerdtfeger, E., I. M. Abdel-Rahim, R. Kardoff, C. Kaiser, D. Franke, J. Schlake, J. Richter, M. Elsheikh, Q. Mohamed-Ali, and J. H. H. Ehrich. 1992. Ultrasonographical investigation of periportal fibrosis in children with Schistosoma mansoni infection: reversibility of morbidity twenty-three months after treatment with praziquantel. Am. J. Trop. Med. Hyg. 46:409-415.
17. Fallon, P. G., E. J. Richardson, G. J. McKenzie, and A. N. J. McKenzie. 2000. Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J. Immunol. 164:2585-2591.
18. Farah, I. O., P. W. Mola, T. M. Kariuki, M. Nyindo, R. E. Blanton, and C. L. King. 2000. Repeated exposure induces periportal fibrosis in Schistosoma mansoni-infected baboons: role of TGF-β and IL-4. J. Immunol. 164:5337-5343.
19. Ferrari, M. L. A., P. M. Z. Coelho, C. M. F. Antunes, C. A. P. Tavares, and A. S. da Cunha. 2003. Efficacy of oxamniquine and praziquantel in the treatment of Schistosoma mansoni infection: a controlled trial. Bull. World Health Org. 81:190-196.
20. Gazzinelli, A., J. Bethony, L. A. Fraga, P. LoVerde, R. Correa-Oliveira, and H. Kloos. 2001. Exposure to Schistosoma mansoni infection in a rural area of Brazil: water contact. Trop. Med. Int. Health 6:126-135.
21. Grogan, J. L., P. G. Kremsner, G. J. van Dam, W. Metzger, B. Mordmüller, A. M. Deelder, and M. Yazdanbakhsh. 1996. Antischistosome IgG4 and IgE responses are affected differentially by chemotherapy in children versus adults. J. Infect. Dis. 173:1242-1247.
22. Henri, S., C. Chevillard, A. Mergani, P. Paris, J. Gaudart, C. Camilla, H. Dessein, F. Montero, N. E. M. A. Elwali, O. K. Saeed, M. Magzoub, and A. J. Dessein. 2002. Cytokine regulation of periportal fibrosis in humans infected with Schistosoma mansoni: IFN-γ is associated with protection against fibrosis and TNF-α with aggravation of disease. J. Immunol. 169:929-936.
23. Homeida, M. A., I. E. Tom, T. Nash, and J. L. Bennett. 1991. Association of the therapeutic activity of praziquantel with the reversal of Symmers' fibrosis induced by Schistosoma mansoni. Am. J. Trop. Med. Hyg. 45:360-365.
24. Jesus, A. R., A. Magalhāes, D. G. Miranda, R. G. Miranda, M. I. Araújo, A. A. De Jesus, A. Silva, L. B. Santana, E. Pearce, and E. M. Carvalho. 2004. Association of type 2 cytokines with hepatic fibrosis in human Schistosoma mansoni infection. Infect. Immun. 72:3391-3397.
25. Kabatereine, N. B., J. Kemijumbi, J. H. Ouma, R. F. Sturrock, A. E. Butterworth, H. Madsen, N. Ornbjerg, D. W. Dunne, and B. J. Vennnervald. 2003. Efficacy and side effects of praziquantel treatment in a highly endemic Schistosoma mansoni focus at Lake Albert, Uganda. Trans. Royal Soc. Trop. Med. Hyg. 97:599-603.
26. Kabatereine, N. B., S. Brooker, A. Koukounari, F. Kazibwe, E. M. Tukahebwa, F. M. Fleming, Y. Zhang, J. P. Webster, J. R. Stothard, and A. Fenwick. 2007. Impact of a national helminth control programme on infection and morbidity in Ugandan schoolchildren. Bull. World Health Org. 85:91-99.
27. Katz, N., A. Chaves, and J. Pellegrino. 1972. A simple device for quantitative stool thick-smear technique in Schistosoma mansoni. Rev. Inst. Med. Trop. São Paulo 14:397-400.
28. Kaviratne, M., M. Hesse, M. Leusink, A. W. Cheever, S. J. Davies, J. H. McKerrow, L. M. Wakefield, J. J. Letterio, and T. A. Wynn. 2004. IL-13 activates a mechanism of tissue fibrosis that is completely TGF-β independent. J. Immunol. 173:4020-4029.
29. Kihara, J. H., N. Muhoho, D. Njomo, I. K. Mwobobia, K. Josyline, Y. Mitsui, T. Awazawa, T. Amano, and C. Mwandawiro. 2007. Drug efficacy of praziquantel and albendazole in school children in Mwea Division, Central Province, Kenya. Acta Trop. 102:165-171.
30. King, C. L., A. Medhat, I. Malhotra, M. Nafeh, A. Helmy, J. Khaudary, S. Ibrahim, M. El-Sherbiny, S. Zaky, R. J. Stupi, K. Brustoski, M. Shehata, and M. T. Shata. 1996. Cytokine control of parasite-specific anergy in human urinary schistosomiasis. IL-10 modulates lymphocyte reactivity. J. Immunol. 156:4715-4721.
31. Kloos, H., J. K. L. Passos, P. LoVerde, R. Correa-Oliveira, and A. Gazzinelli. 2004. Distribution and Schistosoma mansoni infection of Biomphalaria glabrata in different habitats in a rural area in the Jequitinhonha Valley, Minas Gerais, Brazil: environmental and epidemiological aspects. Mem. Inst. Oswaldo Cruz 99:673-681.
32. Lambertucci, J. R., J. Carlos Serufo, R. Gerspacher-Lara, A. A. M. Rayes, R. Teixeira, V. Nobre, and C. M. F. Antunes. 2000. Schistosoma mansoni: assessment of morbidity before and after control. Acta Trop. 77:101-109.
33. Li, Y. S., A. C. Sleigh, Y. Li, M. Tanner, A. Dessein, G. M. Williams, and D. P. Mcmanus. 2002. Five-year impact of repeated praziquantel treatment on subclinical morbidity due to Schistosoma japonicum in China. Trans. Royal Soc. Trop. Med. Hyg. 96:438-443.
34. Magalhães, T. V., G. Gazzinelli, M. C. Alvarez, F. C. Lima e Silva, L. A. Fraga, A. M. Silveira, A. Gazzinelli, J. Bethony, P. Loverde, I. R. Caldas, R. Correa-Oliveira, and A. Prata. 2005. Comparative clinical and ultrasound study of egg-negative and egg-positive individuals from Schistosoma mansoni low morbidity endemic areas, and hospitalized patients with hepatosplenic disease. Rev. Soc. Bras. Med. Trop. 38:33-37.
35. Malaquias, L. C. C., P. L. Falcão, A. M. S. Silveira, G. Gazzinelli, A. Prata, R. L. Coffman, V. Pizziolo, C. P. Souza, D. G. Colley, and R. Correa-Oliveira. 1997. Cytokine regulation of human immune response to Schistosoma mansoni: analysis of the role of IL-4, IL-5 and IL-10 on peripheral blood mononuclear cell responses. Scand. J. Immunol. 46:393-398.
36. Mohamed-Ali, Q., N. E. M. A. Elwali, A. A. Abdelhameed, A. Mergani, S. Rahoud, K. E. Elagib, O. K. Saeed, L. Abel, M. M. A. Magzoub, and A. J. Dessein. 1999. Susceptibility to periportal (Symmers) fibrosis in human Schistosoma mansoni infections: evidence that intensity and duration of infection, gender, and inherited factors are critical in disease progression. J. Infect. Dis. 180:1298-1306.
37. Mola, P. W., I. O. Farah, T. M. Kariuki, M. Nyindo, R. E. Blanton, and C. L. King. 1999. Cytokine control of the granulomatous response in Schistosoma mansoni-infected baboons: role of exposure and treatment. Infect. Immun. 67:6565-6571.
38. Montenegro, S. M., P. Miranda, S. Mahanty, F. G. Abath, K. M. Teixeira, E. M. Coutinho, J. Brinkman, I. Gonçalves, L. A. Domingues, A. Sher, and T. A. Wynn. 1999. Cytokine production in acute versus chronic human schistosomiasis mansoni: the cross-regulatory role of interferon-gamma and interleukin-10 in the responses of peripheral blood mononuclear cells and splenocytes to parasite antigens. J. Infect. Dis. 179:1502-1514.
39. Moukoko, C. E., N. El-Wali, O. K. Saeed, Q. M. Ali, J. Gaudart, A. Dessein, and C. Chevillard. 2003. No evidence for a major effect of tumor necrosis factor alpha gene polymorphism in periportal fibrosis caused by S. mansoni infection. Infect. Immun. 71:5456-5460.
40. Mutapi, F., P. D. Ndhlovu, P. Hagan, J. T. Spicer, T. Mduluza, C. M. R. Turner, S. K. Chandiwana, and M. E. J. Woolhouse. 1998. Chemotherapy accelerates the development of acquired immune responses to Schistosoma haematobium infection. J. Infect. Dis. 178:289-293.
41. Reiman, R. M., R. W. Thompson, C. G. Feng, D. Hari, R. Knight, A. W. Cheever, H. F. Rosenberg, and T. A. Wynn. 2006. Interleukin-5 (IL-5) augments the progression of liver fibrosis by regulating IL-13 activity. Infect. Immun. 74:1471-1479.
42. Reimert, C. L., C. M. Fitzsimmons, S. Joseph, J. K. Mwatha, F. M. Jones, G. Kimani, K. F. Hoffmann, M. Booth, N. B. Kabatereine, D. W. Dunne, and B. J. Vennervald. 2006. Eosinophil activity in Schistosoma mansoni infections in vivo and in vitro in relation to plasma cytokine profile pre-and post-treatment with praziquantel. Clin. Vaccine Immunol. 13:584-593.
43. Silveira, A. M. S., G. Gazzinelli, L. F. Alves-Oliveira, J. Bethony, A. Gazzinelli, C. Carvalho-Queiroz, M. C. B. Alvarez, F. C. Lima-Silva, A. Prata, P. T. LoVerde, and R. Correa-Oliveira. 2004. Human schistosomiasis mansoni: intensity of infection differentially affects the production of interleukin-10, interferon-γ and interleukin-13 by soluble egg antigen or adult worm antigen stimulated cultures. Trans. Royal Soc. Trop. Med. Hyg. 98:514-519.
44. Singh, K. P., H. C. Gerard, A. P. Hudson, and D. L. Boros. 2004. Expression of matrix metalloproteinases and their inhibitors during the resorption of schistosome egg-induced fibrosis in praziquantel-treated mice. Immunology 111:343-352.
45. Talaat, M. R., A. I. El-Bassiouny, A. M. Osman, M. Yossif, R. Charmy, and M. M. Al-Sherbiny. 2007. Cytokine secretion profile associated with periportal fibrosis in S. mansoni-infected Egyptian patients. Parasitol. Res. 101: 289-299.
46. Warren, K. S. 1968. Pathophysiology and pathogenesis of hepatoesplenic schistosomiasis mansoni. Bull. N. Y. Acad. Med. 44:280-294.
47. Warren, K. S. 1979. The pathogenesis of hepatoesplenic schistosomiasis: from man to monkey to mouse to molecule, p. 439-455. In H. Popper and F. Scaffner (ed.), Progress in liver diseases. Grune and Stratton, New York, NY.
48. Zwingenberger, K., G. Harma, H. Feldmeier, O. Muller, A. Steiner, and U. Bienzle. 1988. Liver involvement in human schistosomiasis mansoni. Regression of immunological and biochemical disease markers after specific treatment. Acta Trop. 45:263-275.